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High occurrence of Pacearchaeota and Woesearchaeota (Archaea superphylum DPANN) in the surface waters of oligotrophic high-altitude lakes
Environmental Microbiology Reports
Abstract
We carried out a regional survey on the archaea composition from surface waters of > 300 high altitude Pyrenean lakes (average altitude 2300 m, pH range 4.4-10.1) by 16S rRNA gene tag-sequencing. Relative Archaea abundances ranged between 0 and 6.3% of total prokaryotes amplicons in the PCR mixture, and we detected 769 OTUs (grouped at 97% identity) that split into 13 different lineages, with altitude and pH having a significant effect on the community composition. Woesearchaeota and Pacearchaeota (formerly Euryarchaeota DHVEG-6 cluster) dominated the dataset (83% of total OTUS), showed a high occurrence (presence in c. 75% of the lakes), and had relative abundances significantly and positively correlated with the phylogenetic diversity of bacterial communities. Micrarchaeota-Diapherotrites (formerly Euryarchaeota MEG cluster), Methanomicrobia, Thermoplasmata, and AOA showed relative abundances between 1-3% and occurrences between 14-26%. Minor lineages were SM1K20, Aenigmarchaeota (formerly Euryarchaeota DSEG cluster), Methanobacteria, MCG, and SCG. Environmental preferences substantially differed among lineages, with Aenigmarchaeota and Methanomicrobia having the largest habitat breadth, and Thermoplasmata, AOA and Micrarchaeota the lowest. Pacearchaeota and Woesearchaeota had been mostly reported from saline habitats and sediments, but surface waters of oligotrophic alpine lakes are suitable environments for such ecologically spread and genetically diverse archaeal lineages.
... Moreover, while ultra-small microorganisms have mostly been detected in anoxic environments [69][70][71][72] or cultivated under anoxic conditions [15,25], we found representatives in all oxic groundwaters (>3 mg/L DO) [73] (54/81 samples, Table S1). A few members of DPANN and Patescibacteria lineages have previously been detected in oxic environments [28,67,68,74,75], suggesting a degree of oxygen tolerance (genetic evidence presented below) or that these organisms are concentrated in anoxic niches within the aquifer substrate. ...
... c (Right) Range of all pairwise AAI values (grey) and maximum AAI values (blue) between ultra-small prokaryote MAGs recovered in this study and GTDB representative genomes for a given phylum. Red dashed lines represent the AAI range defining the same family of organisms (45-65%) [74]. The number of genomes included in this analysis is indicated for each phylum in brackets. ...
Aquifers are populated by highly diverse microbial communities, including unusually small bacteria and archaea. The recently described Patescibacteria (or Candidate Phyla Radiation) and DPANN radiation are characterized by ultra-small cell and genomes sizes, resulting in limited metabolic capacities and probable dependency on other organisms to survive. We applied a multi-omics approach to characterize the ultra-small microbial communities over a wide range of aquifer groundwater chemistries. Results expand the known global range of these unusual organisms, demonstrate the wide geographical range of over 11,000 subsurface-adapted Patescibacteria, Dependentiae and DPANN archaea, and indicate that prokaryotes with ultra-small genomes and minimalistic metabolism are a characteristic feature of the terrestrial subsurface. Community composition and metabolic activities were largely shaped by water oxygen content, while highly site-specific relative abundance profiles were driven by a combination of groundwater physicochemistries (pH, nitrate-N, dissolved organic carbon). We provide insights into the activity of ultra-small prokaryotes with evidence that they are major contributors to groundwater community transcriptional activity. Ultra-small prokaryotes exhibited genetic flexibility with respect to groundwater oxygen content, and transcriptionally distinct responses, including proportionally greater transcription invested into amino acid and lipid metabolism and signal transduction in oxic groundwater, along with differences in taxa transcriptionally active. Those associated with sediments differed from planktonic counterparts in species composition and transcriptional activity, and exhibited metabolic adaptations reflecting a surface-associated lifestyle. Finally, results showed that groups of phylogenetically diverse ultra-small organisms co-occurred strongly across sites, indicating shared preferences for groundwater conditions.
... For instance, recently discovered Woesearchaeia, currently also proposed as Ca. Woesearchaeota (Hiraoka et al., 2020), which were predominant in HSB-1 and HSB-2 (Fig. 2E), possesses a high salt tolerance (Huang et al., 2021b;Ortiz-Alvarez and Casamayor, 2016;Wei et al., 2020). The occurrence of Woesearchaeia in different biotopes is summarized in Table S9. ...
... The occurrence of Woesearchaeia in different biotopes is summarized in Table S9. Several studies support that the Woesearchaeia correlates with salinity, consistent with our results (Huang et al., 2021b;Ortiz-Alvarez and Casamayor, 2016;Wei et al., 2020). Nonetheless, Woesearchaeia was also identified in the low salinity environments (Table S9). ...
Intrusion of salinity and petroleum hydrocarbons (e.g., benzene, toluene, ethylbenzene, and xylenes, BTEX) into shallow groundwater by so-called 'produced water' (the water associated with oil and gas production) has recently drawn much attention. However, how this co-contamination affects the groundwater microbial community remains unknown. Herein, geochemical methods (e.g., ion ratios) and high-throughput sequencing (amplicon and shotgun metagenomic) were used to study the contaminant source, hydrogeochemical conditions, microbial community and function in salinity and BTEX co-contaminated shallow groundwater in an oil field, northwest China. The desulfurization coefficient (100rSO4²⁻/rCl⁻), coefficient of sodium and chloride (rNa⁺/rCl⁻), and coefficient of magnesium and chloride (rMg²⁺/rCl⁻) revealed an intrusion of produced water into groundwater, resulting in elevated levels of salinity and BTEX. The consumption of terminal electron acceptors (e.g., NO3⁻, Fe³⁺, and SO4²⁻) was likely coupled with BTEX degradation. Relative to the bacteria, decreased archaeal diversity and enriched community in produced water-contaminated groundwater suggested that archaea were more susceptible to elevated BTEX and salinity. Relative to the nitrate and sulfate reduction genes, the abundance of marker genes encoding fermentation (acetate and hydrogen production) and methanogenesis (aceticlastic and methylotrophic) was more proportional to BTEX concentration. The produced water intrusion significantly enriched the salt-tolerant anaerobic fermentative heterotroph Woesearchaeia in shallow groundwater, and its co-occurrence with BTEX-degrading bacteria and methanogen Methanomicrobia suggested mutualistic interactions among the archaeal and bacterial communities to couple BTEX degradation with fermentation and methanogenesis. This study offers a first insight into the microbial community and function in groundwater contaminated by produced water.
... Therefore, the outcomes of such relations can be described as positive, neutral or negative (Pacheco and Segrè, 2019). For instance, we can cite the parasitic life style for Pacearchaeota and Woesearchaeota with bacteria (Ortiz-Alvarez and Casamayor, 2016). Another contact dependence has also been reported for two archaea, where Nanoarchaeum equitans directly depends on Igniococcus hospitalis for its survival (Hu et al., 2018). ...
... Another contact dependence has also been reported for two archaea, where Nanoarchaeum equitans directly depends on Igniococcus hospitalis for its survival (Hu et al., 2018). This could be explained by the fact that some archaea have a compact genome (Koonin and Wolf, 2008) and limited metabolic capabilities (Ortiz-Alvarez and Casamayor, 2016) so that they could need a partnership to compensate. Another example is provided by some nitrogen-fixing archaea, designated as a single entity which is known to engage an interaction with the bacterial genus Desulfosarcina (Dekas et al., 2009). ...
Bdellovibrio and like organisms (BALOs) are a functional group of Gram-negative bacteria belonging to the classes of Oligoflexia and Alpha-proteobacteria. The main characteristic of BALOs is that they are obligate bacterial predators. In other words, their reproduction and growth depend entirely on the capture of prey, which is not the case for other predatory bacteria for which this mode of survival is optional. Defined by two possible cycles of reproduction, known as periplasmic or epibiotic growth, BALOs seem relatively ubiquitous and their presence has been reported in contrasting environments. As an example, they have been detected, sometimes in high abundance, in soils, fresh and salt water, or in highly anthropized environments such as wastewater treatment plants. Given their attributes, BALOs could exert a significant biological control over microbial populations, particularly on pathogenic bacteria.To date, the majority of studies on the diversity, distribution and quantitative importance of BALOs have been carried out in soils and salt water. Our work, through the C-BALO project has consisted in exploring mainly fresh waters, represented here by the natural large and deep peri-alpine lakes (Annecy, Bourget and Geneva), but also two marine sites (SOLA and MOLA in the Bay of Banyuls, NW Med. Sea). C-BALO aimed at examining, on different time and space scales, the ubiquity, diversity, quantitative importance and potential functional role of the main families of BALOs of the Oligoflexia group. To do so, we employed various molecular biology and microbiology techniques. An important work has focused on the design and testing of a new set of primers specific to BALOs. This work was performed to take into account recent advances in BALOs classification and for an application in high throughput sequencing and quantitative PCR. We were then able to reveal that Bdellovibrionaceae, Peredibacteraceae and Bacteriovoracaceae are present in all the studied habitats. Moreover, that they were characterized by different patterns and marked dynamics, with Peredibacteraceae being the most abundant family and Bacteriovoracaceae the least abundant. In parallel, we were able to reveal an unsuspected diversity within BALOs, especially for Peredibacteraceae and Bdellovibrionaceae, which encompassed more than a hundred OTUs. Furthermore, abundance and diversity of BALOs seemed to be poorly dependent on environmental variables (e.g., physico-chemical parameters), suggesting the importance of biotic interactions such as quantity and quality of prey, competition for prey, predation by flagellates and ciliates, or parasitism by phages, the latter we show to possibly have a significant impact on the dynamics of BALOs. Finally, a few active members of the Bdellovibrionaceae family were isolated from Lake Geneva, again pointing to an important impact of this group of bacteria in the control of bacterial populations, a functional role that has yet to be clarified.
... This super-phylum is estimated to account for approximately half of all the archaeal diversity of the planet [10]. DPANN Archaea have been detected in diverse environments, including subsurface aquifers [11,12], fresh [13], marine [14] and hypersaline waters and sediments [15], hydrothermal vents [16], hot springs [17], and thawed permafrost [18,19]. ...
... The large metabolic repertoire within the Woesearchaeota could be predicted given the widespread distribution of this radiation in diverse aquatic systems and the numerous subgroups identified by 16 S rRNA gene analysis [52], but this high taxonomic and functional diversity within a single ecosystem is rare. Nonetheless, similar findings have been reported in oligotrophic stratified lakes [13], marine systems [53] as well as in groundwater [55], suggesting an adaptation of DPANN archaea to constrained and oligotrophic systems. ...
DPANN archaea account for half of the archaeal diversity of the biosphere, but with few cultivated representatives, their metabolic potential and environmental functions are poorly understood. The extreme geochemical and environmental conditions in meromictic ice-capped Lake A, in the Canadian High Arctic, provided an isolated, stratified model ecosystem to resolve the distribution and metabolism of uncultured aquatic DPANN archaea living across extreme redox and salinity gradients, from freshwater oxygenated conditions, to saline, anoxic, sulfidic waters. We recovered 28 metagenome-assembled genomes (MAGs) of DPANN archaea that provided genetic insights into their ecological function. Thiosulfate oxidation potential was detected in aerobic Woesearchaeota , whereas diverse metabolic functions were identified in anaerobic DPANN archaea, including degradation and fermentation of cellular compounds, and sulfide and polysulfide reduction. We also found evidence for “vampiristic” metabolism in several MAGs, with genes coding for pore-forming toxins, peptidoglycan degradation, and RNA scavenging. The vampiristic MAGs co-occurred with other DPANNs having complementary metabolic capacities, leading to the possibility that DPANN form interspecific consortia that recycle microbial carbon, nutrients and complex molecules through a DPANN archaeal shunt, adding hidden novel complexity to anaerobic microbial food webs.
... In contrast to Yongle, however, the deepest AJ communities were dominated by a recently described archaeal lineage, the Woesearchaeota [9]. Woesearchaeota have been detected in a wide variety of biomes, including groundwater, terrestrial and marine sediments, wetlands, deep-sea hydrothermal vents, and hypersaline lakes [59][60][61][62]. However, their relative abundance is consistently low, at most 5% of the total microbial community in any given environment, with the highest proportions observed in freshwater sediments [61] and high-altitude lakes [62]. ...
... Woesearchaeota have been detected in a wide variety of biomes, including groundwater, terrestrial and marine sediments, wetlands, deep-sea hydrothermal vents, and hypersaline lakes [59][60][61][62]. However, their relative abundance is consistently low, at most 5% of the total microbial community in any given environment, with the highest proportions observed in freshwater sediments [61] and high-altitude lakes [62]. In contrast, Woesearchaeota comprised at least one-third of the blue hole microbiome between 75 and 106 m, reaching a maximum of nearly 60% in the anoxic sulfidic layer in September (Figs. 3 and Fig. 4). ...
... In contrast to Yongle, however, the deepest AJ communities were dominated by a recently described archaeal lineage, the Woesearchaeota [9]. Woesearchaeota have been detected in a wide variety of biomes, including groundwater, terrestrial and marine sediments, wetlands, deep-sea hydrothermal vents, and hypersaline lakes [59][60][61][62]. However, their relative abundance is consistently low, at most 5% of the total microbial community in any given environment, with the highest proportions observed in freshwater sediments [61] and high-altitude lakes [62]. ...
... Woesearchaeota have been detected in a wide variety of biomes, including groundwater, terrestrial and marine sediments, wetlands, deep-sea hydrothermal vents, and hypersaline lakes [59][60][61][62]. However, their relative abundance is consistently low, at most 5% of the total microbial community in any given environment, with the highest proportions observed in freshwater sediments [61] and high-altitude lakes [62]. In contrast, Woesearchaeota comprised at least one-third of the blue hole microbiome between 75 and 106 m, reaching a maximum of nearly 60% in the anoxic sulfidic layer in September (Figs. 3 and Fig. 4). ...
Exploration of oxygen-depleted marine environments has consistently revealed novel microbial taxa and metabolic capabilities that expand our understanding of microbial evolution and ecology. Marine blue holes are shallow karst formations characterized by low oxygen and high organic matter content. They are logistically challenging to sample, and thus our understanding of their biogeochemistry and microbial ecology is limited. We present a metagenomic and geochemical characterization of Amberjack Hole on the Florida continental shelf (Gulf of Mexico). Dissolved oxygen became depleted at the hole’s rim (32 m water depth), remained low but detectable in an intermediate hypoxic zone (40–75 m), and then increased to a secondary peak before falling below detection in the bottom layer (80–110 m), concomitant with increases in nutrients, dissolved iron, and a series of sequentially more reduced sulfur species. Microbial communities in the bottom layer contained heretofore undocumented levels of the recently discovered phylum Woesearchaeota (up to 58% of the community), along with lineages in the bacterial Candidate Phyla Radiation (CPR). Thirty-one high-quality metagenome-assembled genomes (MAGs) showed extensive biochemical capabilities for sulfur and nitrogen cycling, as well as for resisting and respiring arsenic. One uncharacterized gene associated with a CPR lineage differentiated hypoxic from anoxic zone communities. Overall, microbial communities and geochemical profiles were stable across two sampling dates in the spring and fall of 2019. The blue hole habitat is a natural marine laboratory that provides opportunities for sampling taxa with under-characterized but potentially important roles in redox-stratified microbial processes.
... In contrast to Yongle, however, the deepest AJ communities were dominated by a recently described archaeal lineage, the Woesearchaeota [9]. Woesearchaeota have been detected in a wide variety of biomes, including groundwater, terrestrial and marine sediments, wetlands, deep-sea hydrothermal vents, and hypersaline lakes [59][60][61][62]. However, their relative abundance is consistently low, at most 5% of the total microbial community in any given environment, with the highest proportions observed in freshwater sediments [61] and high-altitude lakes [62]. ...
... Woesearchaeota have been detected in a wide variety of biomes, including groundwater, terrestrial and marine sediments, wetlands, deep-sea hydrothermal vents, and hypersaline lakes [59][60][61][62]. However, their relative abundance is consistently low, at most 5% of the total microbial community in any given environment, with the highest proportions observed in freshwater sediments [61] and high-altitude lakes [62]. In contrast, Woesearchaeota comprised at least one-third of the blue hole microbiome between 75 and 106 m, reaching a maximum of nearly 60% in the anoxic sulfidic layer in September (Figs. 3 and Fig. 4). ...
Exploration of oxygen-depleted marine environments has consistently revealed novel microbial taxa and metabolic capabilities that expand our understanding of microbial evolution and ecology. Marine blue holes are shallow karst formations characterized by low oxygen and high organic matter content. They are logistically challenging to sample, and thus our understanding of their biogeochemistry and microbial ecology is limited. We present a metagenomic characterization of Amberjack Hole on the Florida continental shelf (Gulf of Mexico). Dissolved oxygen became depleted at the hole’s rim (32 m water depth), remained low but detectable in an intermediate hypoxic zone (40-75 m), and then increased to a secondary peak before falling below detection in the bottom layer (80-110 m), concomitant with increases in nutrients, dissolved iron, and a series of sequentially more reduced sulfur species. Microbial communities in the bottom layer contained heretofore undocumented levels of the recently discovered phylum Woesearchaeota (up to 58% of the community), along with lineages in the bacterial Candidate Phyla Radiation (CPR). Thirty-one high-quality metagenome-assembled genomes (MAGs) showed extensive biochemical capabilities for sulfur and nitrogen cycling, as well as for resisting and respiring arsenic. One uncharacterized gene associated with a CPR lineage differentiated hypoxic from anoxic zone communities. Overall, microbial communities and geochemical profiles were stable across two sampling dates in the spring and fall of 2019. The blue hole habitat is a natural marine laboratory that provides opportunities for sampling taxa with under-characterized but potentially important roles in redox-stratified microbial processes.
... The phylum Woesearchaeota has been identified in surface waters, sediments, and methane-containing Arctic permafrost [116][117][118], and in wastewater treatment plants [119]. Complete genomes of the representatives reveal that Woesearchaeota is capable of transferring acetyl-CoA to acetate for ATP production using acetate kinase and phosphate acetyltransferase [118], indicating its ability to utilize acetate. ...
... Complete genomes of the representatives reveal that Woesearchaeota is capable of transferring acetyl-CoA to acetate for ATP production using acetate kinase and phosphate acetyltransferase [118], indicating its ability to utilize acetate. Representatives of Woesearchaeota lack genes encoding enzymes needed for many critical metabolic pathways, but possess genes for precursors involved in pathogenesis in bacteria, indicating these archaea might have a symbiotic or parasitic lifestyle [117,118]. In an AD process, the presence of these two phyla might provide extra metabolic pathways linking the use of acetate and methane formation. ...
The use of straw for biofuel production is encouraged by the European Union. A previous study showed the feasibility of producing biomethane in upflow anaerobic sludge blanket (UASB) reactors using hydrolyzed, steam-pretreated wheat straw, before and after dark fermentation with Caldicellulosiruptor saccharolyticus, and lucerne. This study provides information on overall microbial community development in those UASB processes and changes related to acidification. The bacterial and archaeal community in granular samples was analyzed using high-throughput amplicon sequencing. Anaerobic digestion model no. 1 (ADM1) was used to predict the abundance of microbial functional groups. The sequencing results showed decreased richness and diversity in the microbial community, and decreased relative abundance of bacteria in relation to archaea, after process acidification. Canonical correspondence analysis showed significant negative correlations between the concentration of organic acids and three phyla, and positive correlations with seven phyla. Organic loading rate and total COD fed also showed significant correlations with microbial community structure, which changed over time. ADM1 predicted a decrease in acetate degraders after a decrease to pH ≤ 6.5. Acidification had a sustained effect on the microbial community and process performance.
... This result was unexpected, as it is known that archaea thrive under saline conditions due to their high adaptability to extreme conditions (Andrei et al., 2012;Zhao et al., 2022). The same primer pair has been previously used in many microbial diversity surveys which recovered archaeal sequences from oligotrophic high-altitude lakes (Ortiz-Ãlvarez et al., 2020;Ortiz-Alvarez & Casamayor, 2016), inland saline lakes (Ghori et al., 2021;Huang et al., 2020;Menéndez-Serra et al., 2020), and saline sediments under environmental disturbances (S aenz de Miera et al., 2021). However, all the above studies focused on sediment or water samples, which comparatively harbour higher numbers of prokaryotic cells than the woody stems. ...
Inland saline ecosystems suffer multiple stresses (e.g., high radiation, salinity, water scarcity) that may compromise essential ecosystem functions such as organic matter decomposition. Here, we investigated the effects of drought on microbial colonization and decomposition of Sarcocornia fruticosa woody stems across different habitats in a saline watershed: on the dry floodplain, submerged in the stream channel and at the shoreline (first submerged, then emerged). Unexpectedly, weight loss was not enhanced in the submerged stems, while decomposition process differed between habitats. On the floodplain, it was dominated by fungi and high cellulolytic activity; in submerged conditions, a diverse community of bacteria and high ligninolytic activity dominated; and, on the shoreline, enzyme activities were like submerged conditions, but with a fungal community similar to the dry conditions. Results indicate distinct degradation paths being driven by different stress factors: strong water scarcity and photodegradation in dry conditions, and high salinity and reduced oxygen in wet conditions. This suggests that fungi are more resistant to drought, and bacteria to salinity. Overall, in saline watersheds, variations in multiple stress factors exert distinct environmental filters on bacteria and fungi and their role in the decomposition of plant material, affecting carbon cycling and microbial interactions.
... Clearly, the most likely explanation for that variance was the difference in study methods. As a relatively new member of the superphylum DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaea), Woesearchaeota was surprisingly diverse and abundant in a wide range of extreme environments, such as deep oil reservoir, oligo-trophic lakes and indicating a high diversity of their roles in global biogeochemical cycles [34,35]. Recently, multivariate regression analysis further revealed that Woesearchaeota might function in consortium with methanogens in the cycling of carbon [36]. ...
Background
Saline lakes are home to various archaea that play special and crucial roles in the global biogeochemical cycle. The Qinghai-Tibet Plateau hosts a large number of lakes with diverse salinity ranging from 0.1 to over 400 g/L, harboring complex and diverse archaea. To the best of our knowledge, the formation mechanisms and potential ecological roles of archaea in Qinghai-Tibetan Plateau saline lakes remain largely unknown.
Results
Using High-throughput Illumina sequencing, we uncovered the vastly distinct archaea communities between two typical saline lakes with significant salinity differences on the Qinghai Tibet Plateau (Qinghai saline lake and Chaka hypersaline lake) and suggested archaea played different important roles in methanogenesis-related and nitrate reduction-related functions of these two lakes, respectively. Rather than the individual effect of salinity, the composite effect of salinity with diverse environmental parameters (e.g., temperature, chlorophyll a, total nitrogen, and total phosphorus) dominated the explanation of the variations in archaeal community structure in different habitats. Based on the network analysis, we further found the correlations between dominant archaeal OTUs were tight but significantly different between the two habitats, implying that archaeal interactions may also largely determine the shape of archaeal communities.
Conclusion
The present study improved our understanding of the structure and function of archaea in different saline lakes on the Qinghai-Tibet Plateau and provided a new perspective on the mechanisms underlying shaping their communities.
... Archaeal communities were strikingly different between both lakes, with Last Chance dominated by Halobacteria and Nanoarchaeaota [27] and Goodenough Lake composed of a more diverse archaeal community ( Fig. 5A & B). In both lakes, cores taken from close proximity to the underground spring feeding the lakes (core 1) had a markedly different community composition in comparison to other cores ( Fig. 5A & B). ...
Approximately 3.7 billion years ago, microbial life may have emerged in phosphate-rich salty ponds. Surprisingly, analogs of these environments are present in alkaline lake systems, recognized as highly productive biological ecosystems. Investigating the microbial ecology of two Canadian soda lake sediment systems characterized by naturally high phosphate levels. Using a comprehensive approach involving geochemistry, metagenomics, and amplicon sequencing, we discovered that groundwater infiltration into Lake Goodenough sediments supported stratified layers of microbial metabolisms fueled by decaying mats. Effective degradation of microbial mats resulted in unexpectedly low net productivity. Evaporation of water from Last Chance Lake and its sediments led to saturation of brines and a habitat dominated by inorganic precipitation reactions, with low productivity, low organic matter turnover and little biological uptake of phosphorus, leading to high phosphate concentrations. Our research highlights that modern analogs for origin-of-life conditions might be better represented by soda lakes with low phosphate concentrations. Highly alkaline brines were found to be dominated by potentially dormant spore-forming bacteria. These saturated brines also hosted potential symbioses between Halobacteria and Nanoarchaeaota , as well as Lokiarchaea and bacterial sulfate reducers. Metagenome-assembled genomes of Nanoarchaeaota lacked strategies for coping with salty brines and were minimal for Lokiarchaea . Thus, highly alkaline brine environments could be too extreme to support origin of life scenarios. These findings shed light on the complex interplay of microbial life in extreme environments and contribute to our understanding of early Earth environments.
... This result was unexpected, as it is known that archaea thrive under saline conditions due to their high adaptability to extreme conditions (Andrei et al., 2012;Zhao et al., 2022). The same primer pair has been previously used in many microbial diversity surveys which recovered archaeal sequences from oligotrophic high-altitude lakes (Ortiz-Ãlvarez et al., 2020;Ortiz-Alvarez & Casamayor, 2016), inland saline lakes (Ghori et al., 2021;Huang et al., 2020;Menéndez-Serra et al., 2020), and saline sediments under environmental disturbances (S aenz de Miera et al., 2021). However, all the above studies focused on sediment or water samples, which comparatively harbour higher numbers of prokaryotic cells than the woody stems. ...
Mediterranean regions have rivers which are naturally salty and subjected to seasonal droughts. These two stressful environmental conditions can affect the decomposition process of organic matter through affecting fungi and bacteria. The aim of this poster is to describe this effect, and how bacteria and fungi respond differently to these environmental stressors.
... This could suggest that protein evolution in archaea is more sensitive to oxygen levels, whereas bacterial protein sequences may be stronger indicators of redox potential than oxygen. However, we consider the results for archaea to be more uncertain because of limitations of archaea-specific primers (e.g., see reference 32) and the absence from the RefSeq database of representatives of the DPANN superphylum such as Woesearchaeota and Pacearchaeota that are abundant in some environments (118). Across all data sets, the average percentages of genus-level classifications made by the RDP Classifier that were mapped to the NCBI taxonomy are 86% for bacteria and 77% for archaea, suggesting that archaeal communities are not as well represented by available reference proteomes. ...
Despite deep interest in how environments shape microbial communities, whether redox conditions influence the sequence composition of genomes is not well known. We predicted that the carbon oxidation state ( Z C ) of protein sequences would be positively correlated with redox potential (Eh). To test this prediction, we used taxonomic classifications for 68 publicly available 16S rRNA gene sequence data sets to estimate the abundances of archaeal and bacterial genomes in river & seawater, lake & pond, geothermal, hyperalkaline, groundwater, sediment, and soil environments. Locally, Z C of community reference proteomes (i.e., all the protein sequences in each genome, weighted by taxonomic abundances but not by protein abundances) is positively correlated with Eh corrected to pH 7 (Eh7) for the majority of data sets for bacterial communities in each type of environment, and global-scale correlations are positive for bacterial communities in all environments. In contrast, archaeal communities show approximately equal frequencies of positive and negative correlations in individual data sets, and a positive pan-environmental correlation for archaea only emerges after limiting the analysis to samples with reported oxygen concentrations. These results provide empirical evidence that geochemistry modulates genome evolution and may have distinct effects on bacteria and archaea.
IMPORTANCE
The identification of environmental factors that influence the elemental composition of proteins has implications for understanding microbial evolution and biogeography. Millions of years of genome evolution may provide a route for protein sequences to attain incomplete equilibrium with their chemical environment. We developed new tests of this chemical adaptation hypothesis by analyzing trends of the carbon oxidation state of community reference proteomes for microbial communities in local- and global-scale redox gradients. The results provide evidence for widespread environmental shaping of the elemental composition of protein sequences at the community level and establish a rationale for using thermodynamic models as a window into geochemical effects on microbial community assembly and evolution.
... Overall, 26 (15 archaea and 11 bacteria) out of 98 MAGs were the main focus of this research, though these analyses were performed on all 98 microbes of the community. In comparison to bacteria, archaeal biology is still extremely under-explored, and their metabolic and functional potential is not well studied primarily due to the difficulty of culturing them [23][24][25]. Archaea are known to play important roles in hydrothermal vent ecosystems, and throughout the pelagic oceans such as in Fig. 1 Summary of the process followed in studying the Guaymas microbiome. ...
Deep-sea hydrothermal vents are abundant on the ocean floor and play important roles in ocean biogeochemistry. In vent ecosystems such as hydrothermal plumes, microorganisms rely on reduced chemicals and gases in hydrothermal fluids to fuel primary production and form diverse and complex microbial communities. However, microbial interactions that drive these complex microbiomes remain poorly understood. Here, we use microbiomes from the Guaymas Basin hydrothermal system in the Pacific Ocean to shed more light on the key species in these communities and their interactions. We built metabolic models from metagenomically assembled genomes (MAGs) and infer possible metabolic exchanges and horizontal gene transfer (HGT) events within the community. We highlight possible archaea-archaea and archaea-bacteria interactions and their contributions to the robustness of the community. Cellobiose, D-Mannose 1-phosphate, O2, CO2, and H2S were among the most exchanged metabolites. These interactions enhanced the metabolic capabilities of the community by exchange of metabolites that cannot be produced by any other community member. Archaea from the DPANN group stood out as key microbes, benefiting significantly as acceptors in the community. Overall, our study provides key insights into the microbial interactions that drive community structure and organisation in complex hydrothermal plume microbiomes.
... The sequences affiliated with members of the phyla Ca. "Woesearchaeota," Ca. "Thermoplasmatota," and methanogens of the class Methanomicrobia predominated in the sediments, where they were responsible for 6% of the total number of sequences and 92% of all archaeal sequences. Members of the phylum Ca. "Woesearchaeota" are widespread in various aquatic environments, including freshwater and saline lakes (Ortiz-Alvarez and Casamayor, 2016;Kadnikov et al., 2019;Kallistova et al., 2018Kallistova et al., , 2020Savvichev et al., 2020). These archaea are incapable of oxidative metabolism and lack the pathways for synthesis of the major cell components, which may indicate their symbiotic or parasitic lifestyle (Castelle et al., 2015. ...
Eutrophication of lakes results in the intensification of anaerobic processes, including methanogenesis, and therefore in enhanced emission of methane. A littoral area with its variable oxygen regime is the first to react to eutrophication. The diversity of microbial communities in littoral areas is insufficiently studied , and little data are available concerning the methane cycle microorganisms. In this work, the methano-genesis and methane oxidation were investigated in the littoral site of a freshwater temperate Lake Senezh (Russia). A combination of analytical, microbiological and molecular techniques was used, including physicochemical analyses, high-throughput sequencing, potential activity measurements, and cultivation on selective media. The littoral site was found to be an extremely labile ecological niche, which harbors a diverse community containing aerobic, facultative anaerobic and anaerobic microorganisms, both autotrophs and het-erotrophs, which may perform all reactions of the N, S, and CH4 cycles. Methane formation was carried out via hydrogenotrophic, acetoclastic, methylotrophic, and methyl-reducing pathways. Among methanotrophs, type I organisms predominated; type II, nitrate-and nitrite-dependent methanotrophs were also revealed. Comparison of the average rates of methanogenesis and aerobic methane oxidation suggests that all methane, which may potentially be formed in the littoral site of the lake, could simultaneously be oxidized.
... However, despite the high proportion of Thaumarchaeota per sample, the richest groups were Pacearchaeota and Woesearchaeota, considering the whole sampling area but particularly in the canyon. These lineages have an unknown ecological role in the Blanes Canyon system but display an enormous environmental versatility and biome occurrence (Ortiz-Álvarez and Casamayor, 2016). Studies in inland environments support their anaerobic heterotrophic lifestyle and metabolic complementarity with other microbes . ...
... This was consistent with our understanding that association of archaea and bacteria could be based on syntrophic nitrogen cycling (27), where ammonia-oxidizing archaea represent the major drivers of ammonia oxidation (28). Although nitrogen-cycling genes nirK and nosZ were detected in Woesearchaeota (29), studies on the ecological role of Woesearchaeota found that it lacks the important metabolic pathways for the complete tricarboxylic acid cycle (30,31). There might be a potential syntrophic relationship between Woesearchaeota and bacterial members, where bacteria may provide amino acids and other compounds to compensate for the metabolic deficiencies of Woesearchaeota (29) (Fig. S7). ...
Soil microorganisms drive emissions of nitrous oxide from soils; this is a powerful greenhouse gas and the dominant ozone-depleting agent. N 2 O emissions can be partly predicted from soil properties and specific microbial groups, whereas a possible role of below-ground microbial interactions has largely been overlooked.
... Methanogenesis in these ecosystems appear to be driven by biotic interactions with algae communities, or photoautotrophs, which provide acetate or H2, common substrates for methanogens. Woesearchaeota are widespread archaea and are a dominant group in surface aquatic systems [75,76]. Genome reconstructions points to metabolic deficiencies and symbiotic and/or fermentative lifestyles [77]. ...
Groundwater recharge and discharge rates and zones are important hydrogeological characteristics of aquifer systems, yet their impact on the formation of both subterranean and surface microbiomes remains largely unknown. In this study, we used 16S rRNA gene sequencing to characterize and compare the microbial community of seven different aquifers, including the recharge and discharge areas of each system. The connectivity between subsurface and surface microbiomes was evaluated at each site, and the temporal succession of groundwater microbial communities was further assessed at one of the sites. Bacterial and archaeal community composition varied between the different sites, reflecting different geological characteristics, with communities from unconsoli-dated aquifers being distinct from those of consolidated aquifers. Our results also revealed very little to no contribution of surface recharge microbial communities to groundwater communities as well as little to no contribution of groundwater microbial communities to surface discharge communities. Temporal succession suggests seasonal shifts in composition for both bacterial and ar-chaeal communities. This study demonstrates the highly diverse communities of prokaryotes living in aquifer systems, including zones of groundwater recharge and discharge, and highlights the need for further temporal studies with higher resolution to better understand the connectivity between surface and subsurface microbiomes.
... However, we decided to only describe the groups detected, avoiding any interpretations regarding quantity where there could be a strong bias. We detected two main phyla (Fig. S1A); these were Woesearchaeota, a phylum that potentially has a syntrophic interaction with methanogens Ortiz-Alvarez & Casamayor, 2016), and Euryarchaeota, within which we found four halophilic genera: Halovivax, Halorubrum, Halorussus and Haloasta, all of them previously reported in saline habitats and sediments (McGonigle et al., 2019;Zaitseva et al., 2018). In a recent metagenomic study of the Archaean Domes (Medina-Chávez et al., 2019), some archaeal taxa were detected in all sampled sites, forming a "core taxa". ...
We evaluated the microbial diversity and metabolome profile of an uncommon hypersaline elastic microbial mat from Cuatro Ciénegas Basin (CCB) in the Chihuahuan Desert of Coahuila, México. We collected ten samples on a small scale transect (1.5-m) and described its microbial diversity through NGS-based ITS and 16S rDNA gene sequencing. A very low number of taxa comprised a considerable proportion of the mat and were shared across all sampling points, whereas the rare biosphere was more phylogenetically diverse (Faith’s Phylogenetic Diversity (FPD) index) and phylogenetically disperse (using a null model distribution of Phylogenetic Species Clustering (nmdPSC)) than the abundant (high read count) taxa for both analyzed libraries. We also found a distinctive metabolome profile for each sample and were able to tentatively annotate several classes of compounds with relevant biological properties.
... However, pH is often the strongest segregator of community types (55)(56)(57). DNA was extracted, amplified and sequenced with standard methodology as previously described (4,58), using a subset of 224 lake samples where both Bacteria and Eukarya were successfully sequenced. Briefly, high-speed multiplexed rRNA gene sequencing with the Illumina MiSeq System was carried out using the primers 515f and 806r (59) for the bacterial 16S V4 region and the primers 1391f and EukBr for the eukaryal 18S V9 region (60). ...
A fundamental question in biology is why some species tend to occur together in the same locations, while others are never observed to coexist. This question becomes particularly relevant for microorganisms thriving in the highly diluted waters of high mountain lakes, in which biotic interactions might be required to make the most of an extreme environment.
... Group 6, is rather widely distributed in diverse environments (e.g. Castelle et al., 2015;Ortiz-Alvarez and Casamayor, 2016;Han et al., 2017;Xu et al., 2017). In fact, a recent metaanalysis reported a wide diversity of Woesearchaeales subgroups distributed in different ...
Les sédiments marins recouvrent environ 65% de la surface terrestre et les microorganismes qui les peuplent jouent un rôle essentiel dans les cycles biogéochimiques marins. Situés à l’interface entre les communautés pélagiques et de subsurface, les Bactéries et Archées benthiques déterminent la partition entre enfouissement de la matière organique et nutriments relargués dans la colonne d’eau. Comprenant une vaste diversité de microorganismes et des adaptations fonctionnelles spécifiques, elles sont encore peu décrites. Dans le cadre du projet « Pourquoi pas les abysses ? », cette thèse s’est intéressée à la structure et la diversité fonctionnelle des communautés microbiennes benthiques des grands fonds. Dans ce but, nous avons mis en place des méthodes standardisées d’échantillonnage, d’extraction d’ADN et d’analyse bioinformatique. A l’aide de données de métabarcoding 16S, nous avons étudié la biogéographie des communautés de la transition entre Méditerranée et Atlantique, et observé une importante influence de la limitation de dispersion et de la dérive écologique, de façon longitudinale et verticale. Dans les sédiments de surface de deux fosses hadales du Pacifique Sud, la distribution des classes d’Archées dominantes, Nitrososphaerie et Nanoarcheia est influencée par la profondeur et l’horizon sédimentaire, avec plusieurs partenaires putatifs pour la lignée présumée symbiotique des Woesearchaeales. A l’aide de données métagénomiques, nous avons reconstruit 90 MAGs d’Archées de même sédiments, dont 53 affiliés aux Nitrososphaeria dont la variabilité génomique semblent liée à la niche écologique.Dans l’ensemble, les résultats obtenus posent de solides bases pour la caractérisation de la diversité fonctionnelle et des adaptations spécifiques des communautés microbiennes des sédiments marins profonds.
... Based on these findings, the authors proposed that Woesearchaeota probably provide substrates for H 2 /CO 2 -utilizing methanogens and acetate-utilizing methanogens in return for amino acids and other compounds, to compensate for their own metabolic deficiencies. Meanwhile, a positive correlation of the Woesearchaeota relative abundance and bacterial community was reported in a study based on 16S rRNA gene amplicon sequences, suggesting possible interactions between these microbes 19 . ...
The archaeal phylum Woesearchaeota, within the DPANN superphylum, includes phylogenetically diverse microorganisms that inhabit various environments. Their biology is poorly understood due to the lack of cultured isolates. Here, we analyze datasets of Woesearchaeota 16S rRNA gene sequences and metagenome-assembled genomes to infer global distribution patterns, ecological preferences and metabolic capabilities. Phylogenomic analyses indicate that the phylum can be classified into ten subgroups, termed A–J. While a symbiotic lifestyle is predicted for most, some members of subgroup J might be host-independent. The genomes of several Woesearchaeota, including subgroup J, encode putative [FeFe] hydrogenases (known to be important for fermentation in other organisms), suggesting that these archaea might be anaerobic fermentative heterotrophs.
... Aenigmarchaeota", DPANN, symbiont, horizontal gene transfer, cooccurrence network, coevolution network W ith advances in sequencing technologies and bioinformatic approaches, insight into the "unseen majority" prokaryotes has become possible, even when they inhabit complex microbial communities, leading to a tremendous expansion of known archaeal diversity (1)(2)(3)(4)(5)(6)(7). Among recently proposed major archaeal lineages, the Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota (DPANN) superphylum has inspired considerable research attention, which has uncovered their surprisingly small genome sizes, lack of genes associated with core biosynthetic pathways (3,8,9), and extensive phylogenetic and functional diversity (10)(11)(12). "Candidatus Aenigmarchaeota" ("Ca. Aenigmarchaeota"), which represent the "A" of the DPANN superphylum, were first uncovered and named as the "Deep Sea Euryarchaeotic Group (DSEG)" (13). ...
“Candidatus Aenigmarchaeota” (“Ca. Aenigmarchaeota”) represents one of the earliest proposed evolutionary branches within the Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota (DPANN) superphylum. However, their ecological roles and potential host-symbiont interactions are still poorly understood. Here, eight metagenome-assembled genomes (MAGs) were reconstructed from hot spring ecosystems, and further in-depth comparative and evolutionary genomic analyses were conducted on these MAGs and other genomes downloaded from public databases. Although with limited metabolic capacities, we reported that “Ca. Aenigmarchaeota” in thermal environments harbor more genes related to carbohydrate metabolism than “Ca. Aenigmarchaeota” in non- thermal environments. Evolutionary analyses suggested that members from the Thaumarchaeota, Aigarchaeota, Crenarchaeota, and Korarchaeota (TACK) superphylum and Euryarchaeota contribute substantially to the niche expansion of “Ca. Aenigmarchaeota” via horizontal gene transfer (HGT), especially genes related to virus defense and stress responses. Based on co-occurrence network results and recent genetic exchanges among community members, we conjectured that “Ca. Aenigmarchaeota” may be symbionts associated with one MAG affiliated with the genus Pyrobaculum, though host specificity might be wide and variable across different “Ca. Aenigmarchaeota” organisms. This study provides significant insight into possible DPANN-host interactions and ecological roles of “Ca. Aenigmarchaeota.”
... One group, groundwater-associated Huberarchaeota, are predicted to be symbionts of the archaeal Altiarchaeota (SM1) based on highly correlated abundance patterns . Recent work has further illuminated the biology, diversity and distribution of these organisms (Ortiz-Alvarez and Casamayor, 2016;Wurch et al., 2016;Krause et al., 2017;Dombrowski et al., 2019;Hamm et al., 2019), now often referred to as the DPANN (Rinke et al., 2013). Genomic analyses were used to propose that lateral gene transfer, including from bacteria, has shaped the inventories of acidophilic nanoarchaea (Baker et al., 2010). ...
DPANN are small-celled archaea that are generally predicted to be symbionts, and in some cases are known episymbionts of other archaea. As the monophyly of the DPANN remains uncertain, we hypothesized that proteome content could reveal relationships among DPANN lineages, constrain genetic overlap with bacteria, and illustrate how organisms with hybrid bacterial and archaeal protein sets might function. We tested this hypothesis using protein family content that was defined in part using 3,197 genomes including 569 newly reconstructed genomes. Protein family content clearly separates the final set of 390 DPANN genomes from other archaea, paralleling the separation of Candidate Phyla Radiation (CPR) bacteria from all other bacteria. This separation is partly driven by hypothetical proteins, some of which may be symbiosis-related. Pacearchaeota with the most limited predicted metabolic capacities have Form II/III and III-like Rubisco, suggesting metabolisms based on scavenged nucleotides. Intriguingly, the Pacearchaeota and Woesearchaeota with the smallest genomes also tend to encode large extracellular murein-like lytic transglycosylase domain proteins that may bind and degrade components of bacterial cell walls, indicating that some might be episymbionts of bacteria. The pathway for biosynthesis of bacterial isoprenoids is widespread in Woesearchaeota genomes and is encoded in proximity to genes involved in bacterial fatty acids synthesis. Surprisingly, in some DPANN genomes we identified a pathway for synthesis of queuosine, an unusual nucleotide in tRNAs of bacteria. Other bacterial systems are predicted to be involved in protein refolding. For example, many DPANN have the complete bacterial DnaK-DnaJ-GrpE system and many Woesearchaeota and Pacearchaeota possess bacterial group I chaperones. Thus, many DPANN appear to have mechanisms to ensure efficient protein folding of both archaeal and laterally acquired bacterial proteins.
... Ecological studies started to shed light on distribution patterns (Auguet et al., 2010;Hugoni et al., 2015;MacLeod et al., 2019), yet knowledge about the ecological roles of most Archaea remains scarce (Meng et al., 2014;Castelle et al., 2015). Aquatic Archaea are known from a wide variety of habitats like costal (Rios-Del Toro et al., 2018) and deep sea sediments (Lloyd et al., 2013), freshwater (Ortiz-Alvarez and Casamayor, 2016) and pelagic environments (Karner et al., 2001). In most benthic environments, they are less abundant than bacteria, yet their numbers seem to increase with sediment depth (Lipp et al., 2008). ...
Subterranean estuaries (STEs) play an important role in linking nutrient cycling between marine and terrestrial systems. As being the primary drivers of nutrient cycling, the composition of microbial communities and their adaptation toward both, terrestrial and marine conditions are of special interest. While bacterial communities of STEs have received increasing scientific attention, archaeal and meiofaunal diversity was mostly neglected. Previous studies at the investigated sampling site, the STE of a mesotidal beach at the German North Sea island of Spiekeroog, focused on spatial and seasonal patterns of geochemical and bacterial diversity. By additionally investigating the archaeal and meiofaunal diversity and distribution, we now aimed to fill this gap of knowledge to understand the microbial response to submarine groundwater discharge (SGD). The topography of Spiekeroog beach and associated geochemical gradients in porewater displayed a distinct cross-shore zonation, with seawater infiltration on the upper beach at the high water line (HWL), and saline and brackish porewater exfiltration (SGD) at the ridge-runnel structure and the low water line (LWL) on the lower beach. This led to a higher evenness of prokaryotic communities in lower beach areas impacted by SGD compared to unimpacted areas. Archaea contributed 1–4% to the 16S rRNA gene sequence dataset. Those were dominated by Nitrosopumilaceae, corresponding well to higher concentrations of NH4⁺ in the discharge area of the STE. The unimpacted sites had elevated abundances of Wosearchaeia, which were also detected previously in impacted areas of an STE at Mobile Bay (Gulf of Mexico). While a large proportion of prokaryotes were present in the entire intertidal area, meiofaunal community compositions were site specific and dominated by nematodes. Nematode communities of the high-water line differed distinctively from the other sites. Overall, our data indicates that the three domains of life display distinctly different adaptations when facing the same conditions within the STE. Therefore, distribution patterns of any domain can only be understood if all of them, together with basic environmental information are investigated in an integrated context.
... We also found a significant relationship between BC diversity and altitude, with high-altitude lakes having higher microbial diversity. A similar relationship was also reported in other studies that postulated that altitude reflects important changes both biotic and abiotic characteristics (Ortiz-Alvarez and Casamayor, 2016;Siles and Margesin, 2016). Moreover, the lake MEC composition explained 20% of BC beta diversity, indicating interactions between bacteria and micro-eukaryotes (i.e. ...
The aquatic bacterial community (BC) plays a vital role in determining the nature and rate of ecosystem function. However, the biotic and abiotic factors influencing BC structure and function are largely unknown. Hence, the current study characterizes the impact of biotic and abiotic factors on aquatic bacterial biodiversity to determine whether the dominant effects are biotic or abiotic by partitioning their relative effects across temperate Canadian lakes. We collected water samples from sixty southern Ontario lakes and characterized their BC and microbial eukaryotic community (MEC) compositions using high throughput metabarcode sequencing of 16S and 18S rRNA gene fragments. The diversity and richness of aquatic BCs differed considerably among our study lakes, and those differences were explained by environmental, spatial, and biotic (MEC) factors (31%, 23%, and 23% of variance explained, respectively). The relatively large contribution from biotic and abiotic factors (54%), relative to spatial effects, shows deterministic processes prevail in shaping BC assembly in freshwater lakes. However, spatial effects also contributed significantly, highlighting the role of stochastic processes (ecological drift and coupled with limited dispersal) in shaping BC structure. Furthermore, our co-occurrence network analysis showed strong positive and negative interactions within and between the BCs and MECs, indicating mutualistic or antagonistic co-occurrence patterns relationships play important roles in driving the variation in BC composition among our sampled lakes. Considered together, our community analyses show that deterministic and stochastic processes combined contribute to determining the aquatic BC composition, and hence likely function as well, across a broad array of temperate freshwater lakes.
... Several studies have investigated archaeal communities in salt lakes or salterns and observed that they are dominated by the phyla Euryarchaeota, Crenarchaeota, Thaumarchaeota, Pacearchaeota, and Woesearchaeota, albeit with varying relative abundances Najjari et al. 2015;Liu et al. 2016a, b;Ortiz-Alvarez and Casamayor 2016). Taxonomic distributions within archaeal communities are influenced by hypersaline environmental parameters, and variable taxonomic co-occurrence patterns have been observed among different niches. ...
Halophilic Archaea are widely distributed globally in hypersaline environments. However, little is known of how dominant halophilic archaeal genera are distributed across environments and how they may co-associate across ecosystems. Here, the archaeal community composition and diversity from hypersaline environments (> 300 g/L salinity; total of 33 samples) in the Qaidam Basin of China were investigated using high-throughput Illumina sequencing of 16S rRNA genes. The archaeal communities (total of 3,419 OTUs) were dominated by the class Halobacteria (31.7–99.6% relative abundances) within the phylum Euryarchaeota (90.8–99.9%). Five predominant taxa, including Halorubrum, Halobacterium, Halopenitus, Methanothrix, and Halomicrobium, were observed across most samples. However, several distinct genera were associated with individual samples and were inconsistently distributed across samples, which contrast with previous studies of hypersaline archaeal communities. Additionally, co-occurrence network analysis indicated that five network clusters were present and potentially reflective of interspecies interactions among the environments, including three clusters (clusters II, III, and IV) comprising halophilic archaeal taxa within the Halobacteriaceae and Haloferacaceae families. In addition, two other clusters (clusters I and V) were identified that comprised methanogens. Finally, salinity comprising ionic concentrations (in the order of Na⁺ > Ca²⁺ > Mg²⁺) and pH were most correlated with taxonomic distributions across sample sites.
... One group, groundwater-associated Huberarchaeota, are predicted to be symbionts of the archaeal Altiarchaeota (SM1) based on highly correlated abundance patterns . Recent work has further illuminated the biology, diversity and distribution of these organisms (Ortiz-Alvarez and Casamayor, 2016;Wurch et al., 2016;Krause et al., 2017;Dombrowski et al., 2019;Hamm et al., 2019) , now often referred to as the DPANN (Rinke et al., 2013a) . Genomic analyses were used to propose that lateral gene transfer, including from bacteria, has shaped the inventories of acidophilic nanoarchaea (Baker et al., 2010) . ...
DPANN are small-celled archaea that are generally predicted to be symbionts, and in some cases are known episymbionts of other archaea. As the monophyly of the DPANN remains uncertain, we hypothesized that proteome content could reveal relationships among DPANN lineages, constrain genetic overlap with bacteria, and illustrate how organisms with hybrid bacterial and archaeal protein sets might function. We tested this hypothesis using protein family content that was defined in part using 569 newly reconstructed genomes. Protein family content clearly separates DPANN from other archaea, paralleling the separation of Candidate Phyla Radiation (CPR) bacteria from all other bacteria. This separation is partly driven by hypothetical proteins, some of which may be symbiosis-related. Pacearchaeota with the most limited predicted metabolic capacities have Form II/III and III-like Rubisco, suggesting metabolisms based on scavenged nucleotides. Intriguingly, the Pacearchaeota and Woesearchaeota with the smallest genomes also tend to encode large extracellular murein-like lytic transglycosylase domain proteins that may bind and degrade components of bacterial cell walls, indicating that some might be episymbionts of bacteria. The pathway for biosynthesis of bacterial isoprenoids is widespread in Woesearchaeota genomes and is encoded in proximity to genes involved in bacterial fatty acids synthesis. Surprisingly, in some DPANN genomes we identified a pathway for synthesis of queuosine, an unusual nucleotide in tRNAs of bacteria. Other bacterial systems are predicted to be involved in protein refolding. For example, many DPANN have the complete bacterial DnaK-DnaJ-GrpE system and many Woesearchaeota and Pacearchaeota possess bacterial group I chaperones. Thus, many DPANN appear to have mechanisms to ensure efficient protein folding of both archaeal and laterally acquired bacterial proteins.
... Nowadays studies of microbiome often give credence to the analysis of 16S ribosomal RNA sequences for the taxonomic identification of bacterial and archaeal strains. Approximately 1600 base pairs long are present on 16S rRNA gene which includes nine hypervariable regions of various conservation (v1-v9) (Handelsman, 2004;Ortiz-Alvarez et al., 2016). More conservative regions are useful for determining the higher-ranking taxa, whereas more quickly evolving ones can help identify genus or species. ...
... Therefore, the outcomes of such relations can be described as positive, neutral or negative (Pacheco and Segrè, 2019). For instance, we can cite the parasitic life style for Pacearchaeota and Woesearchaeota with bacteria (Ortiz-Alvarez and Casamayor, 2016). Another contact dependence has also been reported for two archaea, where Nanoarchaeum equitans directly depends on Igniococcus hospitalis for its survival (Hu et al., 2018). ...
The diversity and relationships between Archaea and Bacteria remain poorly examined in lakes. Using universal primers targeting 16S rRNA gene via Hiseq sequencing, we explored archaeal and bacterial diversity, structure and relationships in the largest natural deep lake in Western Europe, i.e., Lake Geneva. Despite being less diverse than bacteria, archaeal dominant OTUs assigned to the phylum Thaumarchaeota and Nanoarchaeota displayed significant links with a variety of nitrifying bacteria and other bacteria as suggested by co-occurrence networks and function profile predictions. We propose that archaeal OTUs are most likely involved in nitrogen and methanogen cycles, and formed a consortium with other bacteria that also operate these cycles in the deep layers of the lake. These probable syntrophic or mutualistic associations suggest that dominant archaeal OTUs share with some bacteria a similar niche for mutual benefits.
... Although evidences are not conclusive, but studies where Woesearchaeota members were detected after re-analysis (Table S1) all have V4 region in common. Even other environments such as hydrothermal vents, ocean sediments, groundwater, freshwater lakes and permafrost where Woesearchaeota members were reported also included V4 region (Castelle et al. 2015;Durbin and Teske 2010;Ortiz-Alvarez and Casamayor 2016;Shcherbakova et al. 2016;Takai and Horikoshi 1999). And those where regions other than V4 were used, for example the V6-V8 or the V1-V3 regions were targeted such as in the hypersaline Russian and Mexican lakes respectively, no Woesearchaeota members were detected, even after re-analysis. ...
Inland athalassohaline solar salterns provide unique opportunity to study microbial successions along salinity gradients that resemble transition in natural hypersaline lakes. We analyzed for the first time 16S rRNA gene amplicon sequences of bacteria (V1–V2) and archaea (V4–V5) in saltern brines of India’s largest inland hypersaline Sambhar Lake. Brines of the salterns (S1–S4) are alkaline (pH 9.5–10.5) with salinities of 130, 170, 280 and 350 gL−1 respectively. 16S rRNA gene copynumber of archaea outnumbered that of bacteria in all salterns. Their diversity also increased along S1 through S4, while that of bacteria decreased. Brines of S3 and S4 were dominated by specialized extreme halophilic bacterial (Halanaerobiales, Rhodothermaceae) and archaeal (Halobacteriales, Haloferacales) members with recognized salt-in strategy for osmoadaptation. Microbial assemblages positively correlated to saltern pH, total salinity, and ionic composition. Archaea in S1 and S2 were unprecedentedly represented by poorly known as-yet uncultivated groups, Woesearchaeota (90.35–93.51%) and Nanohaloarchaeota that belong to the newly proposed nano-sized superphylum DPANN. In fact, these taxa were identified in archaeal datasets of other athalassohaline salterns after re-analysis using latest RDP database. Thus, microbial compositions in hypersaline lakes are complex and need revisit particularly for their archaeal diversity to understand their hitherto unknown ecological function in extreme environments.
... Members of the DPANN superphylum, mainly Woesearchaeota, were the predominant archaeal group responsible for up to 50% of all 16S rRNA gene sequences. Members of the DPANN superphylum (Rinke et al., 2013) are widespread in various aquatic ecosystems, including boreal and subarctic lakes (Restrepo-Ortiz and Casamayor, 2013;Ortiz-Alvarez and Casamayor, 2016;Carnevali et al., 2018;Kadnikov et al., 2019b;Kallistova et al., 2019). ...
Microbiological, molecular ecological, biogeochemical, and isotope geochemical research was carried out at the polar Lake Bol’shie Khruslomeny at the coast of the Kandalaksha Bay, White Sea in March and September 2017. The uppermost mixolimnion was oxic, with low salinity (3–5%). The lower chemocline layer was brown-green colored, with very high content of particulate organic matter (up to 11.8 mg C L–1). The lowermost monimolimnion had marine salinity (22–24%) and very high concentrations of sulfide (up to 18 mmol L–1) and CH4 (up to 1.8 mmol L–1). In the chemocline, total microbial abundance and the rate of anoxygenic photosynthesis were 8.8 × 106 cells mL–1 and 34.4 μmol C L–1 day–1, respectively. Both in March and September, sulfate reduction rate increased with depth, peaking (up to 0.6–1.1 μmol S L–1 day–1) in the lower chemocline. Methane oxidation rates in the chemocline were up to 85 and 180 nmol CH4 L–1 day–1 in March and September, respectively; stimulation of this process by light was observed in September. The percentages of cyanobacteria and methanotrophs in the layer where light-induced methane oxidation occurred were similar, ∼2.5% of the microbial community. Light did not stimulate methane oxidation in deeper layers. The carbon isotope composition of particulate organic matter (δ13C-Corg), dissolved carbonates (δ13C-DIC), and methane (δ13C- CH4) indicated high microbial activity in the chemocline. Analysis of the 16S rRNA gene sequences revealed predominance of Cyanobium cyanobacteria (order Synechococcales) in the mixolimnion. Green sulfur bacteria Chlorobium phaeovibrioides capable of anoxygenic photosynthesis constituted ∼20% of the chemocline community both in March and in September. Methyloprofundus gammaptoteobacteria (family Methylomonaceae) were present in the upper chemocline, where active methane oxidation occurred. During winter, cyanobacteria were less abundant in the chemocline, while methanotrophs occurred in higher horizons, including the under-ice layer. Chemolithotrophic gammaproteobacteria of the genus Thiomicrorhabdus, oxidizing reduced sulfur compounds at low oxygen concentrations, were revealed in the chemocline in March. Both in March and September archaea constituted up to 50% of all microorganisms in the hypolimnion. The percentage of putative methanogens in the archaeal community was low, and they occurred mainly in near-bottom horizons.
... A meta-analysis on diverse sequence datasets has revealed that the oxic status of the source environment is a major factor shaping their community composition 47 . This group was dominant (83% of total OTUs) in the water column of fully oxic, oligotrophic Pyrinean lakes 48 . The oxic conditions prevailing in our lentic waterbody from the tail to the dam probably favoured their dominance within the archaeal communities. ...
Spatial heterogeneity along river networks is interrupted by dams, affecting the transport, processing, and storage of organic matter, as well as the distribution of biota. We here investigated the structure of planktonic (free-living, FL), particle-attached (PA) and sediment-associated (SD) bacterial and archaeal communities within a small reservoir. We combined targeted-amplicon sequencing of bacterial and archaeal 16S rRNA genes in the DNA and RNA community fractions from FL, PA and SD, followed by imputed functional metagenomics, in order to unveil differences in their potential metabolic capabilities within the reservoir (tail, mid, and dam sections) and lifestyles (FL, PA, SD). Both bacterial and archaeal communities were structured according to their life-style preferences rather than to their location in the reservoir. Bacterial communities were richer and more diverse when attached to particles or inhabiting the sediment, while Archaea showed an opposing trend. Differences between PA and FL bacterial communities were consistent at functional level, the PA community showing higher potential capacity to degrade complex carbohydrates, aromatic compounds, and proteinaceous materials. Our results stressed that particle-attached prokaryotes were phylogenetically and metabolically distinct from their free-living counterparts, and that performed as hotspots for organic matter processing within the small reservoir.
Archaea are important components of marine microorganisms and widely distributed in various marine environments. They play vital roles in the biogeochemical cycles and the evolution of life on Earth. Up to now, archaea include 4 superphyla (Euryarchaeota, TACK, Asgard, and DPANN) and about 30 different phyla. To provide clues and ideas for further research on archaea from coastal or hadal sediments, this review summarizes the recent progresses on the distribution and metabolic features of four common archaeal groups, including Bathyarchaeota, Woesearchaeota, Asgard archaea, and Thermoprofundales (Marine Benthic Group D).
Previous single-gene surveys using 16S rRNA gene-based methods have revealed the phylogenetic classification, distribution, and diversity of as-yet uncultivated microbial lineages in diverse environments. In particular, archaeal communities associated with high-temperature terrestrial hot springs and sediments are dominated by novel thermophilic and hyperthermophilic populations whose physiological characters and ecological roles are unknown. Recent advances in metagenomic approaches and computational processing of huge volumes of DNA sequence data have further unveiled the evolutionary importance of uncultivated hot spring archaeal lineages and previously undescribed roles in biogeochemical cycles of carbon, nitrogen, sulfur, and metals. In this review article, the uncultured thermophilic and hyperthermophilic archaeal lineages that have accelerated our understanding of the tree of life are illustrated.
Continental freshwater systems are particularly vulnerable to environmental variation. Climate change‐induced desertification and the anthropogenic exploitation of hydric resources result in the progressive evaporation and salinization of inland water bodies in many areas of the globe. However, how this process impacts microbial communities and their activities in biogeochemical cycles is poorly known. Here, we take a space‐for‐time substitution approach and characterize the prokaryotic and eukaryotic microbial communities of two planktonic cell‐size fractions (0.2–5 μm and 5–30 μm) from lakes of diverse trophic levels sampled along a salinity‐alkalinity gradient located in the Trans‐Mexican Volcanic Belt (TMVB). We applied a 16S/18S rRNA gene metabarcoding strategy to determine the microbial community composition of 54 samples from 12 different lakes, from the low‐salinity lake Zirahuén to the hypersaline residual ponds of Rincón de Parangueo. Except for systems at both extremes of the salinity gradient, most lakes along the evaporation trend bear actively forming microbialites, which harbor microbial communities clearly distinct from those of plankton. Several lakes were sampled in winter and late spring and the crater lakes Alchichica and Atexcac were sampled across the water column. Physicochemical parameters related to salinity‐alkalinity were the most influential drivers of microbial community structure whereas trophic status, depth, or season were less important. Our results suggest that climate change and anthropogenic‐induced hydric deficit could significantly affect microbial communities, potentially altering ecosystem functioning.
This research is the first study focusing to explore the diversity of Archaea and methanogens in sediments of 19 selected lakes nearby the Czech polar station on James Ross Island (JRI), Antarctica. The 16S rRNA gene sequencing provided a general view of a diversity of archaeal members and the mcrA gene sequencing has offered deeper insight into the taxonomical diversity of methanogens. Archaea rarely exceeded 1% of the total prokaryotic community. Genera Methanothrix and Methanosarcina were found as the predominating methanogenic members in the lake samples. For the first time in Antarctica, sequences of representatives belonging to Methanothermobacter sp. and Methanomassiliicoccales , and a high proportion of sequences belonging to Methanoperedens -like archaea, methanotrophs that couples anaerobic methane oxidation to denitrification, were recorded. The presence of the genus Methanobacterium has been also captured for the first time to a such large extent. Individual lakes from one area shared much higher similarity in their methanogenic diversity with the lakes from another area rather than with the lakes within the same area, suggesting that a lake location will be not the main factor influencing the diversity of the methanogens. Our research unambiguously provides evidence that the lakes of the JRI and surrounding islands are a potential source of new archaeal species.
Trillions of microorganisms, including bacteria, archaea, fungi, and viruses, live in or on the human body. Microbe-microbe and microbe-host interactions are often influenced by diffusible and microbe-associated small molecules. Over the past few years, it has become evident that these interactions have a substantial impact on human health and disease. In this Perspective, we summarize the research involving the discovery of methanogenic and non-methanogenic archaea associated with the human body. In particular, we emphasize the importance of some archaeal metabolites in mediating intra- and interspecies interactions in the ecological environment of the human body. A deep understanding of the archaeal metabolites as well as their biological functions may reveal in more detail whether and how archaea are involved in maintaining human health and/or causing certain diseases.
Brines at or near the surface of present-day Mars are a potential explanation for seasonally recurring dark streaks on the walls of craters, termed recurring slope lineae (RSL). Deliquescence and freezing point depression are possible drivers of brine stability, attributable to the high salinity observed in martian regolith including chlorides and perchlorates. Investigation of life, which may inhabit RSL, and the cellular mechanisms necessary for survival, must consider the tolerance of highly variable hydration, freeze-thaw cycles, and high osmolarity in addition to the anaerobic, oligotrophic, and irradiated environment. We propose the saltpan, an ephemeral, hypersaline wetland as an analogue for putative RSL hydrology. Saltpan sediment archaeal and bacterial communities showed tolerance of the Mars-analogous atmosphere, hydration, minerology, salinity, and temperature. Although active growth and a shift to well-adapted taxa were observed, susceptibility to low-concentration chloride and perchlorate addition suggested that such a composition was insufficient for beneficial water retention relative to added salt stress.
Bantang hot spring is natural, geologically formed by the aggregation of both cold and hot spring water. For the first time, this study combined 16S rRNA genes high-throughput sequencing and bioinformatics analyses to determine the prokaryotic microbe diversity and community structure in the water. A total of 5266 OTUs were obtained, and the community of water was found to comprise 32 bacterial phyla with the most abundant phylum of members belonging to Proteobacteria, and six archaeal phyla with the most abundant phylum of members belonging to Woesearchaeota. Alphaproteobacteria, Burkholderiales, and Comamonadaceae were the highest represented classified species at the level of class, order, and family, respectively. The most abundant bacterial and archaeal genus were Subdivision3 genera incertae sedis and Pacearchaeota Incertae Sedis AR13, and more than a quarter of microorganisms were unclassified genus. Among the top 50 most abundant OTUs, 18 OTUs including the earliest and latest species in evolution have not yet been classified. In the COG analysis, ‘General function prediction only’ was found to be the highest represented category, whereas among predicted KEGG pathways, ‘Membrane Transport’ was the most abundant. Thus, findings from this study greatly improve our understanding to explore novel microorganisms in future.
Little is known about the microbial diversity of rivers that flow across the changing subarctic landscape. Using amplicon sequencing (rRNA and rRNA genes) combined with HPLC pigment analysis and physicochemical measurements, we investigated the diversity of two size fractions of planktonic Bacteria, Archaea and microbial eukaryotes along environmental gradients in the Great Whale River (GWR), Canada. This large subarctic river drains an extensive watershed that includes areas of thawing permafrost, and discharges into southeastern Hudson Bay as an extensive plume that gradually mixes with the coastal marine waters. The microbial communities differed by size-fraction (separated with a 3-μm filter), and clustered into three distinct environmental groups: (1) the GWR sites throughout a 150-km sampling transect; (2) the GWR plume in Hudson Bay; and (3) small rivers that flow through degraded permafrost landscapes. There was a downstream increase in taxonomic richness along the GWR, suggesting that sub-catchment inputs influence microbial community structure in the absence of sharp environmental gradients. Microbial community structure shifted across the salinity gradient within the plume, with changes in taxonomic composition and diversity. Rivers flowing through degraded permafrost had distinct physicochemical and microbiome characteristics, with allochthonous dissolved organic carbon explaining part of the variation in community structure. Finally, our analyses of the core microbiome indicated that while a substantial part of all communities consisted of generalists, most taxa had a more limited environmental range and may therefore be sensitive to ongoing change.
Thermodynamics predicts a positive correlation between environmental redox potential and oxidation state of molecules; if found for microbial communities it would imply a new kind of deterministic eco-evolutionary process. This study examines evidence for local- and global-scale correlations between oxidation-reduction potential (ORP or Eh) in environmental samples and carbon oxidation state ( Z C ) of estimated bacterial and archaeal community proteomes. Seventy-nine public datasets for seven environment types (river & seawater, lake & pond, alkaline spring, hot spring, groundwater, sediment, and soil) were analyzed. Taxonomic abundances inferred from high-throughput 16S rRNA gene sequences were combined with NCBI Reference Sequence (RefSeq) proteomes to estimate the amino acid compositions and chemical formulas (C c H h N n O o S s ) of community proteomes, which yield Z C . Alkaline hot springs have the lowest Z C for both bacterial and archaeal domains of any environment. Positive global correlations between redox potential and Z C are found for bacterial communities in lake & pond, groundwater, and soil environments, but not archaeal communities, suggesting a broad ecological signal of chemical shaping in Bacteria.
Archaea, one of the three domains of life along with Bacteria and Eukarya, contains ancient life forms such as methanogen that are observed today on Earth, and one lineage Asgard archaea is also considered the closest ancestor of Eukarya. Recently, with the development of interdisciplinary studies from Earth and Life sciences, archaeal organisms are considered to play pivotal roles in geochemical cycling in nature. However, our understanding of the attributes, origin and evolution, geochemical and ecological functions of Archaea is hampered by the scarcity of archaeal isolates, which has represented a challenge to researchers for the last 40 years. Cultivation-independent sequencing and phylogenomic analyses have demonstrated a considerable diversity of Archaea with more than 20 novel phyla. However, only four archaeal phyla have cultured representatives, leaving large gaps in our knowledge of the metabolic capabilities and ecological functions of the majority of archaeal strains identified exclusively by DNA sequencing. In this review, we summarize the discovery and development of archaeal research, highlight the knowledge gap between uncultured and cultured archaeal microbes, and call on the importance of devoting greater research efforts to archaeal cultivation. Finally, we outlined new ideas and strategic approaches, namely, (1) genome-based methods, (2) microbial network information-based methods, (3) genome-scale model-guided methods, and (4) machine learning methods, to enable the cultivation of uncultivated archaeal microbes using accumulated high-throughput sequencing data. © 2021, Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature.
The domain Archaea is a key research model for gaining insights into the origin and evolution of life, as well as the relevant biogeochemical processes. The discovery of nanosized DPANN archaea has overthrown many aspects of microbiology.
We evaluated the microbial diversity and metabolomic signatures of a hypersaline elastic microbial mat from Cuatro Cienegas Basin (CCB) in the Chihuahuan Desert of Coahuila, Mexico. We collected ten samples within a small scale (1.5-meters transect) and found a high microbial diversity through NGS-based ITS and 16S rRNA gene sequencing. A very low number of taxa were abundant and shared between all sites, whereas the rare biosphere was more phylogenetically diverse (FPD index) and phylogenetically disperse (PSC index) than the abundant taxa for both analyzed libraries. In regard to potential biotic interactions (Pearson analysis), there were more positive correlations than negative. We also found a distinctive metabolomic signature for each sample and were able to tentatively annotate several classes of compounds with relevant biological properties. Together, these results reveal cohesive, diverse and fluctuating microbial communities, where abundant and rare taxa appear to have different ecological roles.
Due to their unique metabolism and important ecological roles, deep-sea hydrothermal archaea have attracted great scientific interests. Among these archaea, DPANN superphylum archaea are widely distributed in hydrothermal vent environments. However, DPANN metabolism and ecology remain largely unknown. In this study, we assembled 20 DPANN genomes among 43 reconstructed genomes obtained from deep-sea hydrothermal vent sediments. Phylogenetic analysis suggests 6 phyla, comprised of Aenigmarchaeota, Diapherotrites, Nanoarchaeota, Pacearchaeota, Woesearchaeota and a new candidate phylum we have designated Kexuearchaeota. These are included in the 20 DPANN archaeal members, indicating their broad diversity in this special environment. Analyses on their metabolism reveal deficiencies due to their reduced genome size, including gluconeogenesis and de novo nucleotide and amino acid biosynthesis. However, DPANN archaea possess alternate strategies to address these deficiencies. DPANN archaea also have potentials to assimilate nitrogen and sulfur compounds, indicating a potentially important ecological role in the hydrothermal vent system.
IMPORTANCE
DPANN archaea show high distribution in the hydrothermal system though they display small genome size and some incomplete biological processes. Exploring their metabolism is helpful to understand how such small forms of life adapt to this unique environment and what ecological roles they play. In this study, we obtained 20 high quality metagenome-assembled genomes (MAGs) corresponding to 6 phyla of the DPANN group (Aenigmarchaeota, Diapherotrites, Nanoarchaeota, Pacearchaeota, Woesearchaeota and a new candidate phylum designated Kexuearchaeota). Further metagenomic analyses provided insights on the metabolism and ecological functions of DPANN archaea to adapt to deep-sea hydrothermal environments. Our study contributes to gain a deeper understanding of their special lifestyles and should provide clues to cultivate this important archaeal group in the future.
Woesearchaeota as a newly established member of the superphylum DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota and Nanohaloarchaea) are surprisingly abundant and diverse in a wide variety of environments, including deep oil reservoir, sulfuric springs and anoxic aquifers, indicating a high diversity of their roles in global biogeochemical cycles. However, ecological functions of them remain elusive. To fill up this gap, we analyzed and compared the global distribution patterns of Woesearchaeota using the genomes available publicly. As a result, both ecological distribution patterns and metabolic predictions support a key role of woesearchaeotal lineages in cycling of carbon, nitrogen, and sulfur. Multivariate regression analysis reveals that Woesearchaeota might function in consortium with methanogens in the cycling of carbon in anaerobic environments, particularly in soils or sediments. Moreover, comparative genomic analysis and ecological distribution suggest the potential roles of Woesearchaeota in the processes of denitrification, nitrogen fixation, and dissimilatory nitrite reduction, especially in the wastewater treatment systems; and also uncovered the potential capability of sulfate reduction, sulfide oxidation and thiosulfate oxidation in sulfuric or sulfidic-rich environments. Our findings add more information into the ecological roles of archaea in the anoxic environment.
We performed coenzyme factor 430 (F430) analysis and radiocarbon measurements to identify deep microorganisms, including methanogenic archaea, and assess the origin of methane in a deep organic- and iodine-rich aquifer in a forearc basin at the Southern Kanto gas field, Boso Peninsula, Japan. We detected high concentrations of native F430 (approximately 1.67 × 10⁴ femto mol L–1) in the absence of the F430 epimer. Both lipid and small-subunit rRNA gene analyses indicated that the biomass of domain archaea was less than 10% of the total prokaryotes, while methanogenic archaea (e.g., Methanomicrobia) was detected in the rRNA sequences. These results strongly suggest high active methanogenesis potential mediated by the subsurface microbes. A stable carbon isotope ratio of methane (δ¹³Cmethane, −67.9 to −71.4‰ vs Vienna Pee Dee Belemnite) and a huge reservoir of high-purity methane (>99%) indicated a typical biogenic origin. Radiocarbon measurements of methane and dissolved inorganic carbon (DIC) revealed ¹⁴C-depleted (both Δ¹⁴Cmethane and Δ¹⁴CDIC, <−997.4‰), suggesting that the entire deep habitat and methanogenesis represents an isolated subterranean microbial ecosystem.
We have applied a global analytical approach to uncultured Archaea that for the first time reveals well-defined community patterns along broad environmental gradients and habitat types. Phylogenetic patterns and the environmental factors governing the creation and maintenance of these patterns were analyzed for c. 2000 archaeal 16S rRNA gene sequences from 67 globally distributed studies. The sequences were dereplicated at 97% identity, grouped into seven habitat types, and analyzed with both Unifrac (to explore shared phylogenetic history) and multivariate regression tree (that considers the relative abundance of the lineages or taxa) approaches. Both phylogenetic and taxon-based approaches showed salinity and not temperature as one of the principal driving forces at the global scale. Hydrothermal vents and planktonic freshwater habitats emerged as the largest reservoirs of archaeal diversity and consequently are promising environments for the discovery of new archaeal lineages. Conversely, soils were more phylo- genetically clustered and archaeal diversity was the result of a high number of closely related phylotypes rather than different lineages. Applying the ecological concept of ‘indicator species’, we detected up to 13 indicator archaeal lineages for the seven habitats prospected. Some of these lineages (that is, hypersaline MSBL1, marine sediment FCG1 and freshwater plSA1), for which ecological importance has remained unseen to date, deserve further attention as they represent potential key archaeal groups in terms of distribution and ecological processes. Hydrothermal vents held the highest number of indicator lineages, suggesting it would be the earliest habitat colonized by Archaea. Overall, our approach provided ecological support for the often arbitrary nomenclature within uncultured Archaea, as well as phylogeographical clues on key ecological and evolutionary aspects of archaeal biology.
Members of the archaeal Miscellaneous Crenarchaeotic Group (MCG) are among the most successful microorganisms on the planet. During its evolutionary diversification, this very diverse group has managed to cross the saline-freshwater boundary, one of the most important evolutionary barriers structuring microbial communities. However, the current understanding on the ecological significance of MCG in freshwater habitats is scarce and the evolutionary relationships between freshwater and saline MCG remains poorly known. Here, we carried out molecular phylogenies using publicly available 16S rRNA gene sequences from various geographic locations to investigate the distribution of MCG in freshwater and saline sediments and to evaluate the implications of saline-freshwater transitions during the diversification events. Our approach provided a robust ecological framework in which MCG archaea appeared as a core generalist group in the sediment realm. However, the analysis of the complex intragroup phylogeny of the 21 subgroups currently forming the MCG lineage revealed that distinct evolutionary MCG subgroups have arisen in marine and freshwater sediments suggesting the occurrence of adaptive evolution specific to each habitat. The ancestral state reconstruction analysis indicated that this segregation was mainly due to the occurrence of a few saline-freshwater transition events during the MCG diversification. In addition, a network analysis showed that both saline and freshwater MCG recurrently co-occur with archaea of the class Thermoplasmata in sediment ecosystems, suggesting a potentially relevant trophic connection between the two clades.The ISME Journal advance online publication, 18 August 2015; doi:10.1038/ismej.2015.143.
High-throughput sequencing of small subunit ribosomal RNA (SSU rRNA) genes from marine environments is a widely applied method used to uncover the composition of microbial communities. We conducted an analysis of surface ocean waters with the commonly employed hypervariable 4 region SSU rRNA gene primers 515F and 806R, and found that bacteria belonging to the SAR11 clade of Alphaproteobacteria, a group typically making up 20 to 40% of the bacterioplankton in this environment, were greatly underrepresented and comprised <4% of the total community. Using the SILVA reference database, we found a single nucleotide mismatch to nearly all SAR11 subclades, and revised the 806R primer so that it increased the detection of SAR11 clade sequences in the database from 2.6 to 96.7%. We then compared the performance of the original and revised 806R primers in surface seawater samples, and found that SAR11 comprised 0.3 to 3.9% of sequences with the original primers and 17.5 to 30.5% of the sequences with the revised 806R primer. Furthermore, an investigation of seawater obtained from aquaria re vealed that SAR11 sequences acquired with the revised 806R primer were more similar to natural cellular abundances of SAR11 detected using fluorescence in situ hybridization counts. Collectively, these results demonstrate that a minor adjustment to the 806R primer will greatly increase detection of the globally abundant SAR11 clade in marine and lake environments, and enable inclusion of this important bacterial lineage in experimental and environmental-based studies.
The zonation of anaerobic methane-cycling Archaea in hydrothermal sediment of Guaymas Basin was studied by general primer pairs (mcrI, ME1/ME2, mcrIRD) targeting the alpha subunit of methyl coenzyme M reductase gene (mcrA) and by new group- specific mcrA and 16S rRNA gene primer pairs. The mcrIRD primer pair outperformed the other general mcrA primer pairs in detection sensitivity and phylogenetic coverage. Methanotrophic ANME-1 Archaea were the only group detected with group- specific primers only. The detection of 14 mcrA lineages surpasses the diversity previously found in this location. Most phylo- types have high sequence similarities to hydrogenotrophs, methylotrophs, and anaerobic methanotrophs previously detected at Guaymas Basin or at hydrothermal vents, cold seeps, and oil reservoirs worldwide. Additionally, five mcrA phylotypes belonging to newly defined lineages are detected. Two of these belong to deeply branching new orders, while the others are new species or genera of Methanopyraceae and Methermicoccaceae. Downcore diversity decreases from all groups detected in the upper 6 cm (2 to 40°C, sulfate measurable to 4 cm) to only two groups below 6 cm (>40°C). Despite the presence of hyperthermophilic genera (Methanopyrus, Methanocaldococcus) in cooler surface strata, no genes were detected below 10 cm (>60°C). While mcrA- based and 16S rRNA gene-based community compositions are generally congruent, the deeply branching mcrA cannot be as- signed to specific 16S rRNA gene lineages. Our study indicates that even among well-studied metabolic groups and in previously characterized model environments, major evolutionary branches are overlooked. Detecting these groups by improved molecular biological methods is a crucial first step toward understanding their roles in nature.
Significance
An archaeal origin for eukaryotes is an exciting recent finding. Nevertheless, it has been based largely on the reconstruction of universal trees. The use of an alternative strategy based on markers shared between Archaea and eukaryotes and Archaea and Bacteria bypasses potential problems linked to the analysis of the three domains simultaneously. Comparison of the phylogenies obtained by these two complementary sets of markers supports a sister relationship between eukaryotes and the Thaumarchaeota/“Aigarchaeota” (candidate phylum)/Crenarchaeota/Korarchaeota lineage but also robustly indicates a root of the tree of Archaea that challenges the traditional topology of this domain. This sensibly changes our perspective of the ancient evolution of the Archaea, early life, and Earth.
The zonation of anaerobic methane-cycling Archaea in hydrothermal sediment of Guaymas Basin was studied by general primer pairs (mcrI, ME1/ME2, mcrIRD), targeting the alpha subunit of methyl coenzyme M reductase gene (mcrA), and by new group-specific mcrA and 16S rRNA gene primer pairs. The mcrIRD outperformed the other general mcrA primer pairs in detection sensitivity and phylogenetic coverage. Methanotrophic ANME-1 Archaea were the only group only detected with group-specific primers. The detection of 14 mcrA lineages surpasses the diversity previously found in this location. Most phylotypes have high sequence similarities to hydrogenotrophs, methylotrophs and anaerobic methanotrophs previously detected at Guaymas Basin or at hydrothermal vents, cold seeps, and oil reservoirs worldwide. Additionally, five mcrA phylotypes belonging to newly defined lineages are detected. Two of these belong to deeply-branching new orders, while the others are new species or genera of Methanopyraceae and Methermicoccaceae. Downcore diversity decreases, from all groups detected in the upper 6 cm (∼2-40°C, sulfate measurable to 4 cm), to only two groups below 6 cm (>40°C). Despite the presence of hyperthermophilic genera (Methanopyrus, -caldococcus) in cooler surface strata, no genes were detected below 10 cm (≥60°C). While mcrA and 16S rRNA gene-based community composition are generally congruent, the deeply-branching mcrA cannot be assigned to specific 16S rRNA gene lineages. Our study indicates that even among well-studied metabolic groups, and in previously characterized model environments, major evolutionary branches are overlooked. Detecting these groups by improved molecular biological methods is a crucial first step toward understanding their roles in nature.
Copyright © 2014, American Society for Microbiology. All Rights Reserved.
Deep lakes are of specific interest in the study of archaeal assemblages as chemical stratification in the water column allows niche differentiation and distinct community structure. Active archaeal community and potential nitrifiers were investigated monthly over one year by pyrosequencing 16S rRNA transcripts and genes, and by quantification of archaeal amoA genes in two deep lakes. Our results showed that the active archaeal community patterns of spatial and temporal distribution were different between these lakes. The meromictic lake characterized by a stable redox gradient but variability in nutrient concentrations, exhibited large temporal rearrangements of the dominant euryarchaeal phylotypes, suggesting a variety of ecological niches and dynamic archaeal communities in the hypolimnion of this lake. Conversely, Thaumarchaeota MGI largely dominated in the second lake where deeper water layers exhibited only short periods of complete anoxia and constant low ammonia concentrations. Investigations conducted on archaeal amoA transcripts abundance suggested that not all lacustrine Thaumarchaeota conduct the process of nitrification. A high number of 16S rRNA transcripts associated to crenarchaeal group C3 or the Miscellaneous Euryarchaeotic Group indicates the potential for these uncharacterized groups to contribute to nutrient cycling in lakes.
This article is protected by copyright. All rights reserved.
Current hypotheses about the history of cellular life are mainly based on analyses of cultivated organisms, but these represent only a small fraction of extant biodiversity. The sequencing of new environmental lineages therefore provides an opportunity to test, revise or reject existing ideas about the tree of life and the origin of eukaryotes. According to the textbook three-domains hypothesis, the eukaryotes emerge as the sister group to a monophyletic Archaea. However, recent analyses incorporating better phylogenetic models and an improved sampling of the archaeal domain have generally supported the competing eocyte hypothesis, in which core genes of eukaryotic cells originated from within the Archaea, with important implications for eukaryogenesis. Given this trend, it was surprising that a recent analysis incorporating new genomes from uncultivated Archaea recovered a strongly supported three-domains tree. Here, we show that this result was due in part to the use of a poorly-fitting phylogenetic model and also to the inclusion by an automated pipeline of genes of putative bacterial origin rather than nucleo-cytosolic versions for some of the eukaryotes analyzed. When these issues were resolved, analyses including the new archaeal lineages placed core eukaryotic genes within the Archaea. These results are consistent with a number of recent studies in which improved archaeal sampling and better phylogenetic models agree in supporting the "eocyte" tree over the three domains hypothesis.
Quantitative environmental distribution of two widely distributed uncultured freshwater Euryarchaeota with unknown functional role was explored by newly designed quantitative PCR primers targeting the 16S rRNA gene of clades Miscellaneous Euryarchaeota Group (MEG, containing the groups pMC2A384 and VALII/Eury4) and Deep-Sea Euryarchaeotal Groups (DSEG, targeting the cluster named VALIII containing the DHVE-3/DSEG, BC07-2A-27/DSEG-3 and DSEG-2 groups), respectively. The summer surface plankton of 28 lakes was analysed, and one additional dimictic deep alpine lake, Lake Redon, was temporally and vertically surveyed covering seasonal limnological variability. A trophic range between 0.2 and 5.2 μg l(-1) Chl a, and pH span from 3.8 to 9.5 was explored at altitudes between 632 and 2590 m above sea level. The primers showed to be highly selective with c. 85% coverage and 100% specificity. Only pH significantly explained the changes observed in gene abundances and environment. In Lake Redon, DSEG bloomed in deep stratified waters both in summer and early spring, and MEG at intermediate depths during the ice-cover period. Overall, MEG and DSEG showed a differential ecological distribution although correlational analyses indicated lack of coupling of both Euryarchaeota with phytoplankton (chlorophyll a). However, an intriguing positive and significant relationship was found between DSEG and putative ammonia oxidizing thaumarchaeota.
The Integrated Microbial Genomes (IMG) data warehouse integrates genomes from all three domains of life, as well as plasmids,
viruses and genome fragments. IMG provides tools for analyzing and reviewing the structural and functional annotations of
genomes in a comparative context. IMG’s data content and analytical capabilities have increased continuously since its first
version released in 2005. Since the last report published in the 2012 NAR Database Issue, IMG’s annotation and data integration
pipelines have evolved while new tools have been added for recording and analyzing single cell genomes, RNA Seq and biosynthetic
cluster data. Different IMG datamarts provide support for the analysis of publicly available genomes (IMG/W: http://img.jgi.doe.gov/w), expert review of genome annotations (IMG/ER: http://img.jgi.doe.gov/er) and teaching and training in the area of microbial genome analysis (IMG/EDU: http://img.jgi.doe.gov/edu).
The Miscellaneous Crenarchaeota group (MCG) Archaea is one of the predominant archaeal groups in anoxic environments and may have significant roles in the global biogeochemical cycles. However, no isolate of MCG has been cultivated or characterized to date. In this study, we investigated the genetic organization, ecophysiological properties and evolutionary relationships of MCG archaea with other archaeal members using metagenome information and the result of gene expression experiments. A comparison of the gene organizations and similarities around the 16S rRNA genes from all available MCG fosmid and cosmid clones revealed no significant synteny among genomic fragments, demonstrating that there are large genetic variations within members of the MCG. Phylogenetic analyses of large-subunit+small-subunit rRNA, concatenated ribosomal protein genes and topoisomerases IB gene (TopoIB) all demonstrate that MCG constituted a sister lineage to the newly proposed archaeal phylum Aigarchaeota and Thaumarchaeota. Genes involved in protocatechuate degradation and chemotaxis were found in a MCG fosmid 75G8 genome fragment, suggesting that this MCG member may have a role in the degradation of aromatic compounds. Moreover, the expression of a putative 4-carboxymuconolactone decarboxylase was observed when the sediment was supplemented with protocatechuate, further supporting the hypothesis that this MCG member degrades aromatic compounds.The ISME Journal advance online publication, 10 October 2013; doi:10.1038/ismej.2013.174.
Genome sequencing enhances our understanding of the biological world by providing blueprints for the evolutionary and functional diversity that shapes the biosphere. However, microbial genomes that are currently available are of limited phylogenetic breadth, owing to our historical inability to cultivate most microorganisms in the laboratory. We apply single-cell genomics to target and sequence 201 uncultivated archaeal and bacterial cells from nine diverse habitats belonging to 29 major mostly uncharted branches of the tree of life, so-called 'microbial dark matter'. With this additional genomic information, we are able to resolve many intra- and inter-phylum-level relationships and to propose two new superphyla. We uncover unexpected metabolic features that extend our understanding of biology and challenge established boundaries between the three domains of life. These include a novel amino acid use for the opal stop codon, an archaeal-type purine synthesis in Bacteria and complete sigma factors in Archaea similar to those in Bacteria. The single-cell genomes also served to phylogenetically anchor up to 20% of metagenomic reads in some habitats, facilitating organism-level interpretation of ecosystem function. This study greatly expands the genomic representation of the tree of life and provides a systematic step towards a better understanding of biological evolution on our planet.
The annual dynamics of three different ammonia-oxidizing archaea (AOA) ecotypes (amoA gene) and of the SAGMGC-1 (Nitrosotalea-like aquatic Thaumarchaeota) group (16S rRNA gene) were studied by newly designed specific primers and quantitative polymerase chain reaction analysis in a deep oligotrophic high mountain lake (Lake Redon, Limnological Observatory of the Pyrenees, Spain). We observed segregated distributions of the main AOA populations, peaking separately in time and space, and under different ammonia concentrations and irradiance conditions. Strong positive correlation in gene abundances was found along the annual survey between 16S rRNA SAGMAGC-1 and one of the amoA ecotypes suggesting the potential for ammonia oxidation in the freshwater SAGMAGC-1 clade. We also observed dominance of Nitrosotalea-like ecotypes over Nitrosopumilus-like (Marine Group 1.1a) and not the same annual dynamics for the two thaumarchaeotal clades. The fine scale segregation in space and time of the different AOA ecotypes indicated the presence of phylogenetically close but ecologically segregated AOA species specifically adapted to specific environmental conditions. It remains to be elucidated what would be such environmental drivers.
Rapid advances in sequencing technology have changed the experimental landscape of microbial ecology. In the last 10 years the field has moved from sequencing hundreds of 16S rRNA gene fragments per study using clone libraries to the sequencing of millions of fragments per study using next generation sequencing technologies from 454 and Illumina. As these technologies advance it is critical to assess the strengths, weaknesses and overall suitability of these platforms for the interrogation of microbial communities. Here we present an improved method for sequencing variable regions within the 16S rRNA gene using Illumina's MiSeq platform, which is currently capable of producing paired 250-nt reads. We evaluated three overlapping regions of the 16S rRNA gene that vary in their length (i.e. V34, V4, and V45) by re-sequencing a mock community and natural samples from human feces, mouse feces, and soil. By titrating the concentration of 16S rRNA gene amplicons applied to the flow cell and using a quality score-based approach to correct discrepancies between reads used to construct contigs, we were able to reduce error rates by as much as two orders of magnitude. Finally, we re-processed samples from a previous study to demonstrate that large numbers of samples could be multiplexed and sequenced in parallel with shotgun metagenomes. These analyses demonstrate that our approach can provide data that are at least as good as that generated by the 454 platform while providing considerably higher sequencing coverage for a fraction of the cost.
The Monegros desert contains one of the largest sets of inland saline lakes in Europe constituting a threatened landscape of great scientific and ecological value with large number of reported endemisms. We analyzed bacteria, archaea and microbial eukaryotes from 11 saline lakes in winter and spring by rRNA gene fingerprinting and sequencing covering large salinity (2.7-22.1%) and temperature ranges (1.5-35.3°C). The highest ecological diversity (Shannon-Weaver index) was found in protists and the lowest in Archaea. Eukaryotes showed higher ecological diversity at intermediate salinities, whereas Bacteria and Archaea did not. The genetic diversity was broad and with remarkable novelty. The highest novelty was found in Archaea at the lowest saline concentrations, whereas for bacteria and protists no differences were observed along the gradient. Euryarchaeota of the enigmatic group DHVEG-6 and phylotypes distantly related to well-known haloarchaea were present in several sites. Recurrent presence of bacterial phylotypes distantly related to Psychroflexus and Cryomorphaceae initially isolated from polar marine habitats, was observed. Saline lakes contained chlorophyta, among other new groups, substantially different from green algae previously reported in marine or freshwater. The great scientific and ecological value found for macroorganisms can be extended to the idiosyncratic microbes inhabiting such unique habitat in Europe. This article is protected by copyright. All rights reserved.
Despite their crucial role in the nitrogen cycle, freshwater ecosystems are relatively rarely studied for active ammonia oxidizers (AO). This study of Lake Lucerne determined the abundance of both amoA genes and gene transcripts of ammonia-oxidizing archaea (AOA) and bacteria (AOB) over a period of 16 months, shedding more light on the role of both AO in a deep, alpine lake environment. At the surface, at 42 m water depth, and in the water layer immediately above the sediment, AOA generally outnumbered AOB. However, in the surface water during summer stratification, when both AO were low in abundance, AOB were more numerous than AOA. Temporal distribution patterns of AOA and AOB were comparable. Higher abundances of amoA gene transcripts were observed at the onset and end of summer stratification. In summer, archaeal amoA genes and transcripts correlated negatively with temperature and conductivity. Concentrations of ammonium and oxygen did not vary enough to explain the amoA gene and transcript dynamics. The observed herbivorous zooplankton may have caused a hidden flux of mineralized ammonium and a change in abundance of genes and transcripts. At the surface, AO might have been repressed during summer stratification due to nutrient limitation caused by active phytoplankton.
During the last few years, the analysis of microbial diversity in various habitats greatly increased our knowledge on the kingdom Archaea. At the same time, we became aware of the multiple ways in which Archaea may interact with each other and with organisms of other kingdoms. The large group of euryarchaeal methanogens and their methane oxidizing relatives, in particular, take part in essential steps of the global methane cycle. Both of these processes, which are in reverse to each other, are partially conducted in a symbiotic interaction with different partners, either ciliates and xylophagous animals or sulfate reducing bacteria. Other symbiotic interactions are mostly of unknown ecological significance but depend on highly specific mechanisms. This paper will give an overview on interactions between Archaea and other organisms and will point out the ecological relevance of these symbiotic processes, as long as these have been already recognized.
SILVA (from Latin silva, forest, http://www.arb-silva.de) is a comprehensive web resource for up to date, quality-controlled databases of aligned ribosomal RNA (rRNA) gene sequences
from the Bacteria, Archaea and Eukaryota domains and supplementary online services. The referred database release 111 (July 2012) contains 3 194 778 small subunit
and 288 717 large subunit rRNA gene sequences. Since the initial description of the project, substantial new features have
been introduced, including advanced quality control procedures, an improved rRNA gene aligner, online tools for probe and
primer evaluation and optimized browsing, searching and downloading on the website. Furthermore, the extensively curated SILVA
taxonomy and the new non-redundant SILVA datasets provide an ideal reference for high-throughput classification of data from
next-generation sequencing approaches.
We investigated the spatial distribution and diversity of ammonia-oxidizing Archaea (AOA) across gradients of pH, trophic status, and altitude in a set of high mountain lakes (Limnological Observatory of the Pyrenees, NE Spain). Both phylogeny- and taxonomy-based approaches revealed well-defined AOA community patterns with pH as the main potential driving environmental factor. The I.1a and SAGMGC-1 Thaumarchaeota clusters, and their potentially associated amoA gene variants (clusters Fresh 5 and Soil/Fresh 1, respectively) showed the highest relative abundances in the most oligotrophic lakes. Euryarchaeota (i.e., HV-Fresh cluster, Methanomicrobiales, and Thermoplasmatales) dominated in lakes with higher trophic status. The phylogenetic diversity (PD) in Pyrenean lakes was 1.5 to 2.3 fold higher than the PD from an equivalent number of globally distributed marine and soil sites. We observed segregated distributions for SAGMGC-1, preferently distributed in the lakes with the lowest pH (<5) and the highest nitrite concentration (>0.12 μM), and I.1a in lakes with lower nitrite and dissolved organic carbon concentrations below 0.5 mg/L. Overall, these results showed strong selection by local environmental conditions, unveiled new ecological niches for freshwater SAGMGC-1 in low pH oligotrophic lakes, and suggested specific and successful adaptations of planktonic archaea to the high mountain lakes landscape. © 2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved.
Microorganisms mediating ammonia oxidation play a fundamental role in the connection between biological nitrogen fixation and anaerobic nitrogen losses. Bacteria and Archaea ammonia oxidizers (AOB and AOA, respectively) have colonized similar habitats worldwide. Ammonia oxidation is the rate-limiting step in nitrification, and the ammonia monooxygenase (Amo) is the key enzyme involved. The molecular ecology of this process has been extensively explored by surveying the gene of the subunit A of the Amo (amoA gene). In the present study, we explored the phylogenetic community ecology of AOB and AOA, analyzing 5776 amoA gene sequences from >300 isolation sources, and clustering habitats by environmental ontologies. As a whole, phylogenetic richness was larger in AOA than in AOB, and sediments contained the highest phylogenetic richness whereas marine plankton the lowest. We also observed that freshwater ammonia oxidizers were phylogenetically richer than their marine counterparts. AOA communities were more dissimilar to each other than those of AOB, and consistent monophyletic lineages were observed for sediments, soils, and marine plankton in AOA but not in AOB. The diversification patterns showed a more constant cladogenesis through time for AOB whereas AOA apparently experienced two fast diversification events separated by a long steady-state episode. The diversification rate (γ statistic) for most of the habitats indicated γ(AOA) > γ(AOB). Soil and sediment experienced earlier bursts of diversification whereas habitats usually eutrophic and rich in ammonium such as wastewater and sludge showed accelerated diversification rates towards the present. Overall, this work shows for the first time a global picture of the phylogenetic community structure of both AOB and AOA assemblages following the strictest analytical standards, and provides an ecological view on the differential evolutionary paths experienced by widespread ammonia-oxidizing microorganisms. The emerged picture of AOB and AOA distribution in different habitats provides a new view to understand the ecophysiology of ammonia oxidizers on Earth.
Recent findings indicate that increased atmospheric deposition of nitrogen of human origin has caused changes in the pattern of ecological nutrient limitation in lakes in the northern hemisphere. An increase in the nitrogen to phosphorus ratio, and hence a shift from pristine nitrogen limitation to human-induced phosphorus limitation of phytoplankton growth, seems to have been driven by deposition of atmospheric nitrogen. These findings challenge the classical paradigm of lake phytoplankton productivity being naturally limited by phosphorus availability. However, atmospheric phosphorus deposition may also be highly relevant. Here we show how dissolved inorganic nitrogen concentration has decreased in the Pyrenean lake district over recent decades, despite there being an increase in deposition of atmospheric nitrogen. This is related to an increased atmospheric phosphorus load in the lake water, as a result of higher atmospheric inputs. These changes are causing phytoplankton to revert from being phosphorus-limited to being nitrogen-limited.
16S ribosomal RNA gene (rDNA) amplicon analysis remains the standard approach for the cultivation-independent investigation
of microbial diversity. The accuracy of these analyses depends strongly on the choice of primers. The overall coverage and
phylum spectrum of 175 primers and 512 primer pairs were evaluated in silico with respect to the SILVA 16S/18S rDNA non-redundant reference dataset (SSURef 108 NR). Based on this evaluation a selection
of ‘best available’ primer pairs for Bacteria and Archaea for three amplicon size classes (100–400, 400–1000, ≥1000 bp) is provided. The most promising bacterial primer pair (S-D-Bact-0341-b-S-17/S-D-Bact-0785-a-A-21),
with an amplicon size of 464 bp, was experimentally evaluated by comparing the taxonomic distribution of the 16S rDNA amplicons
with 16S rDNA fragments from directly sequenced metagenomes. The results of this study may be used as a guideline for selecting
primer pairs with the best overall coverage and phylum spectrum for specific applications, therefore reducing the bias in
PCR-based microbial diversity studies.
Examining the patterns of archaeal diversity in little-explored organic-lean marine subsurface sediments presents an opportunity to study the association of phylogenetic affiliation and habitat preference in uncultured marine Archaea. Here we have compiled and re-analyzed published archaeal 16S rRNA clone library datasets across a spectrum of sediment trophic states characterized by a wide range of terminal electron-accepting processes. Our results show that organic-lean marine sediments in deep marine basins and oligotrophic open ocean locations are inhabited by distinct lineages of archaea that are not found in the more frequently studied, organic-rich continental margin sediments. We hypothesize that different combinations of electron donor and acceptor concentrations along the organic-rich/organic-lean spectrum result in distinct archaeal communities, and propose an integrated classification of habitat characteristics and archaeal community structure.
Freshwater habitats have been identified as one of the largest reservoirs of archaeal genetic diversity, with specific lineages of ammonia-oxidizing archaea (AOA) populations different from soils and seas. The ecology and biology of lacustrine AOA is, however, poorly known. In the present study, vertical changes in archaeal abundance by CARD-FISH, quantitative PCR (qPCR) analyses and identity by clone libraries were correlated with environmental parameters in the deep glacial high-altitude Lake Redon. The lake is located in the central Spanish Pyrenees where atmospheric depositions are the main source of reactive nitrogen. Strong correlations were found between abundance of thaumarchaeotal 16S rRNA gene, archaeal amoA gene and nitrite concentrations, indicating an ammonium oxidation potential by these microorganisms. The bacterial amoA gene was not detected. Three depths with potential ammonia-oxidation activity were unveiled along the vertical gradient, (i) on the top of the lake in winter-spring (that is, the 0 (o)C slush layers above the ice-covered sheet), (ii) at the thermocline and (iii) the bottom waters in summer-autumn. Overall, up to 90% of the 16S rRNA gene sequences matched Thaumarchaeota, mostly from both the Marine Group (MG) 1.1a (Nitrosoarchaeum-like) and the sister clade SAGMGC-1 (Nitrosotalea-like). Clone-libraries analysis showed the two clades changed their relative abundances with water depth being higher in surface and lower in depth for SAGMGC-1 than for MG 1.1a, reflecting a vertical phylogenetic segregation. Overall, the relative abundance and recurrent appearance of SAGMGC-1 suggests a significant environmental role of this clade in alpine lakes. These results expand the set of ecological and thermal conditions where Thaumarchaeota are distributed, unveiling vertical positioning in the water column as a key factor to understand the ecology of different thaumarchaeotal clades in lacustrine environments.
Microbial diversity was evaluated in an anoxic zone of Tucuruí Hydroelectric Power Station reservoir in Brazilian Amazonia using a culture-independent approach by amplifying and sequencing fragments of the 16S rRNA gene using metagenomic DNA as a template. Samples obtained from the photic, aphotic (40 m) and sediment (60 m) layers were used to construct six 16S rDNA libraries containing a total of 1,152 clones. The sediment, aphotic and photic layers presented 64, 33 and 35 unique archaeal operational taxonomic units (OTUs). The estimated richness of these layers was evaluated to be 153, 106 and 79 archaeal OTUs, respectively, using the abundance-based coverage estimator (ACE) and 114, 83 and 77 OTUs using the Chao1 estimator. For bacterial sequences, 114, 69 and 57 OTUs were found in the sediment, aphotic and photic layers, which presented estimated richnesses of 1,414, 522 and 197 OTUs (ACE) and 1,059, 1,014 and 148 OTUs (Chao1), respectively. Phylogenetic analyses of the sequences obtained revealed a high richness of microorganisms which participate in the carbon cycle, namely, methanogenic archaea and methanotrophic proteobacteria. Most sequences obtained belong to non-culturable prokaryotes. The present study offers the first glimpse of the huge microbial diversity of an anoxic area of a man-made lacustrine environment in the tropics.
Thaumarchaeota range among the most abundant archaea on Earth. Initially classified as 'mesophilic Crenarchaeota', comparative genomics has recently revealed that they form a separate and deep-branching phylum within the Archaea. This novel phylum comprises in 16S rRNA gene trees not only all known archaeal ammonia oxidizers but also several clusters of environmental sequences representing microorganisms with unknown energy metabolism. Ecophysiological studies of ammonia-oxidizing Thaumarchaeota suggest adaptation to low ammonia concentrations and an autotrophic or possibly mixotrophic lifestyle. Extrapolating from the wide substrate range of copper-containing membrane-bound monooxygenases, to which the thaumarchaeal ammonia monooxygenases belong, the use of substrates other than ammonia for generating energy by some members of the Thaumarchaeota seems likely.
The Yellowstone geothermal complex has yielded foundational discoveries that have significantly enhanced our understanding of the Archaea. This study continues on this theme, examining Yellowstone Lake and its lake floor hydrothermal vents. Significant Archaea novelty and diversity were found associated with two near-surface photic zone environments and two vents that varied in their depth, temperature and geochemical profile. Phylogenetic diversity was assessed using 454-FLX sequencing (~51,000 pyrosequencing reads; V1 and V2 regions) and Sanger sequencing of 200 near-full-length polymerase chain reaction (PCR) clones. Automated classifiers (Ribosomal Database Project (RDP) and Greengenes) were problematic for the 454-FLX reads (wrong domain or phylum), although BLAST analysis of the 454-FLX reads against the phylogenetically placed full-length Sanger sequenced PCR clones proved reliable. Most of the archaeal diversity was associated with vents, and as expected there were differences between the vents and the near-surface photic zone samples. Thaumarchaeota dominated all samples: vent-associated organisms corresponded to the largely uncharacterized Marine Group I, and in surface waters, ~69-84% of the 454-FLX reads matched archaeal clones representing organisms that are Nitrosopumilus maritimus-like (96-97% identity). Importance of the lake nitrogen cycling was also suggested by >5% of the alkaline vent phylotypes being closely related to the nitrifier Candidatus Nitrosocaldus yellowstonii. The Euryarchaeota were primarily related to the uncharacterized environmental clones that make up the Deep Sea Euryarchaeal Group or Deep Sea Hydrothermal Vent Group-6. The phylogenetic parallels of Yellowstone Lake archaea to marine microorganisms provide opportunities to examine interesting evolutionary tracks between freshwater and marine lineages.
We investigated the top 30-cm sediment prokaryotic community structure in 5-cm spatial resolution, at an active site of the Amsterdam mud volcano, East Mediterranean Sea, based on the 16S rRNA gene diversity. A total of 339 and 526 sequences were retrieved, corresponding to 25 and 213 unique (≥98% similarity) phylotypes of Archaea and Bacteria, respectively, in all depths. The Shannon-Wiener diversity index H was higher for Bacteria (1.92-4.03) than for Archaea (0.99-1.91) and varied differently between the two groups. Archaea were dominated by anaerobic methanotrophs ANME-1, -2 and -3 groups and were related to phylotypes involved in anaerobic oxidation of methane from similar habitats. The much more complex Bacteria community consisted of 20 phylogenetic groups at the phylum/candidate division level. Proteobacteria, in particular δ-Proteobacteria, was the dominant group. In most sediment layers, the dominant phylotypes of both the Archaea and Bacteria communities were found in neighbouring layers, suggesting some overlap in species richness. The similarity of certain prokaryotic communities was also depicted by using four different similarity indices. The direct comparison of the retrieved phylotypes with those from the Kazan mud volcano of the same field revealed that 40.0% of the Archaea and 16.9% of the Bacteria phylotypes are common between the two systems. The majority of these phylotypes are closely related to phylotypes originating from other mud volcanoes, implying a degree of endemicity in these systems.
Four stratified basins in Lake Kivu (Rwanda-Democratic Republic of the Congo) were sampled in March 2007 to investigate the
abundance, distribution, and potential biogeochemical role of planktonic archaea. We used fluorescence in situ hybridization with catalyzed-reported deposition microscopic counts (CARD-FISH), denaturing gradient gel electrophoresis
(DGGE) fingerprinting, and quantitative PCR (qPCR) of signature genes for ammonia-oxidizing archaea (16S rRNA for marine Crenarchaeota group 1.1a [MCG1] and ammonia monooxygenase subunit A [amoA]). Abundance of archaea ranged from 1 to 4.5% of total DAPI (4′,6-diamidino-2-phenylindole) counts with maximal concentrations
at the oxic-anoxic transition zone (∼50-m depth). Phylogenetic analysis of the archaeal planktonic community revealed a higher
level of richness of crenarchaeal 16S rRNA gene sequences (21 of the 28 operational taxonomic units [OTUs] identified [75%])
over euryarchaeotal ones (7 OTUs). Sequences affiliated with the kingdom Euryarchaeota were mainly recovered from the anoxic water compartment and mostly grouped into methanogenic lineages (Methanosarcinales and Methanocellales). In turn, crenarchaeal phylotypes were recovered throughout the sampled epipelagic waters (0- to 100-m depth), with clear
phylogenetic segregation along the transition from oxic to anoxic water masses. Thus, whereas in the anoxic hypolimnion crenarchaeotal
OTUs were mainly assigned to the miscellaneous crenarchaeotic group, the OTUs from the oxic-anoxic transition and above belonged
to Crenarchaeota groups 1.1a and 1.1b, two lineages containing most of the ammonia-oxidizing representatives known so far. The concomitant
vertical distribution of both nitrite and nitrate maxima and the copy numbers of both MCG1 16S rRNA and amoA genes suggest the potential implication of Crenarchaeota in nitrification processes occurring in the epilimnetic waters of the lake.
The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.
We have applied a global analytical approach to uncultured Archaea that for the first time reveals well-defined community patterns along broad environmental gradients and habitat types. Phylogenetic patterns and the environmental factors governing the creation and maintenance of these patterns were analyzed for c. 2000 archaeal 16S rRNA gene sequences from 67 globally distributed studies. The sequences were dereplicated at 97% identity, grouped into seven habitat types, and analyzed with both Unifrac (to explore shared phylogenetic history) and multivariate regression tree (that considers the relative abundance of the lineages or taxa) approaches. Both phylogenetic and taxon-based approaches showed salinity and not temperature as one of the principal driving forces at the global scale. Hydrothermal vents and planktonic freshwater habitats emerged as the largest reservoirs of archaeal diversity and consequently are promising environments for the discovery of new archaeal lineages. Conversely, soils were more phylogenetically clustered and archaeal diversity was the result of a high number of closely related phylotypes rather than different lineages. Applying the ecological concept of 'indicator species', we detected up to 13 indicator archaeal lineages for the seven habitats prospected. Some of these lineages (that is, hypersaline MSBL1, marine sediment FCG1 and freshwater plSA1), for which ecological importance has remained unseen to date, deserve further attention as they represent potential key archaeal groups in terms of distribution and ecological processes. Hydrothermal vents held the highest number of indicator lineages, suggesting it would be the earliest habitat colonized by Archaea. Overall, our approach provided ecological support for the often arbitrary nomenclature within uncultured Archaea, as well as phylogeographical clues on key ecological and evolutionary aspects of archaeal biology.
Motivation: DnaSP is a software package for a comprehensive analysis of DNA polymorphism data. Version 5 implements a number of new features
and analytical methods allowing extensive DNA polymorphism analyses on large datasets. Among other features, the newly implemented
methods allow for: (i) analyses on multiple data files; (ii) haplotype phasing; (iii) analyses on insertion/deletion polymorphism
data; (iv) visualizing sliding window results integrated with available genome annotations in the UCSC browser.
Availability: Freely available to academic users from: http://www.ub.edu/dnasp
Contact: jrozas{at}ub.edu
The Guerrero Negro (GN) hypersaline microbial mats have become one focus for biogeochemical studies of stratified ecosystems. The GN mats are found beneath several of a series of ponds of increasing salinity that make up a solar saltern fed from Pacific Ocean water pumped from the Laguna Ojo de Liebre near GN, Baja California Sur, Mexico. Molecular surveys of the laminated photosynthetic microbial mat below the fourth pond in the series identified an enormous diversity of bacteria in the mat, but archaea have received little attention. To determine the bulk contribution of archaeal phylotypes to the pond 4 study site, we determined the phylogenetic distribution of archaeal rRNA gene sequences in PCR libraries based on nominally universal primers. The ratios of bacterial/archaeal/eukaryotic rRNA genes, 90%/9%/1%, suggest that the archaeal contribution to the metabolic activities of the mat may be significant. To explore the distribution of archaea in the mat, sequences derived using archaeon-specific PCR primers were surveyed in 10 strata of the 6-cm-thick mat. The diversity of archaea overall was substantial albeit less than the diversity observed previously for bacteria. Archaeal diversity, mainly euryarchaeotes, was highest in the uppermost 2 to 3 mm of the mat and decreased rapidly with depth, where crenarchaeotes dominated. Only 3% of the sequences were specifically related to known organisms including methanogens. While some mat archaeal clades corresponded with known chemical gradients, others did not, which is likely explained by heretofore-unrecognized gradients. Some clades did not segregate by depth in the mat, indicating broad metabolic repertoires, undersampling, or both.
The seasonal variations in community structure and cell morphology of pelagic procaryotes from a high mountain lake (Gossenköllesee, Austria) were studied by in situ hybridization with rRNA-targeted fluorescently labeled oligonucleotide probes (FISH) and image-analyzed microscopy. Compositional changes and biomass fluctuations within the assemblage were observed both in summer and beneath the winter ice cover and are discussed in the context of physicochemical and biotic parameters. Proteobacteria of the beta subclass (beta-proteobacteria) formed a dominant fraction of the bacterioplankton (annual mean, 24% of the total counts), whereas alpha-proteobacteria were of similar relative importance only during spring (mean, 11%). Bacteria of the Cytophaga-Flavobacterium cluster, although less abundant, constituted the largest fraction of the filamentous morphotypes during most of the year, thus contributing significantly to the total microbial biomass. Successive peaks of threadlike and rod-shaped archaea were observed during autumn thermal mixing and the period of ice cover formation, respectively. A set of oligonucleotide probes targeted to single phylotypes was constructed from 16S rRNA-encoding gene clone sequences. Three distinct populations of uncultivated microbes, affiliated with the alpha- and beta-proteobacteria, were subsequently monitored by FISH. About one-quarter of all of the beta-proteobacteria (range, 6 to 53%) could be assigned to only two phylotypes. The bacterial populations studied were annually recurrent, seasonally variable, and vertically stratified, except during the periods of lake overturn. Their variability clearly exceeded the fluctuations of the total microbial assemblage, suggesting that the apparent stability of total bacterioplankton abundances may mask highly dynamic community fluctuations.
Microbial community analysis via high-throughput sequencing of amplified 16S rRNA genes is an essential microbiology tool. We found the popular primer pair 515F (515F-C) and 806R greatly underestimated (e.g. SAR11) or overestimated (e.g. Gammaproteobacteria) common marine taxa. We evaluated marine samples and mock communities (containing 11 or 27 marine 16S clones), showing alternative primers 515F-Y (5'- GTGYCAGCMGCCGCGGTAA) and 926R (5'- CCGYCAATTYMTTTRAGTTT) yield more accurate estimates of mock community abundances, produce longer amplicons that can differentiate taxa unresolvable with 515F-C/806R, and amplify eukaryotic 18S rRNA. Mock communities amplified with 515F-Y/926R yielded closer observed community composition vs. expected (r(2) =0.95) compared to 515F-Y/806R (r(2) ∼0.5). Unexpectedly, biases with 515F-Y/806R against SAR11 in field samples (∼4-10-fold) were stronger than in mock communities (∼2-fold). Correcting a mismatch to Thaumarchaea in the 515F-C increased their apparent abundance in field samples, but not as much as using 926R rather than 806R. With plankton samples rich in eukaryotic DNA (>1μm size fraction), 18S sequences averaged ∼17% of all sequences. A single mismatch can strongly bias amplification, but even perfectly matched primers can exhibit preferential amplification. We show that beyond in silico predictions, testing with mock communities and field samples is important in primer selection.
This article is protected by copyright. All rights reserved.
Background: Archaea represent a significant fraction of Earth’s biodiversity, yet they remain much less well understood than Bacteria. Gene surveys, a few metagenomic studies, and some single-cell sequencing projects have revealed numerous little-studied archaeal phyla. Certain lineages appear to branch deeply and may be part of a major phylum radiation. The structure of this radiation and the physiology of the organisms remain almost unknown.
Results: We used genome-resolved metagenomic analyses to investigate the diversity, genomes sizes, metabolic capacities, and potential roles of Archaea in terrestrial subsurface biogeochemical cycles. We sequenced DNA from complex sediment and planktonic consortia from an aquifer adjacent to the Colorado River (USA) and reconstructed the first complete genomes for Archaea using cultivation-independent methods. To provide taxonomic context, we analyzed an additional 151 newly sampled archaeal sequences. We resolved two new phyla within a major, apparently deep-branching group of phyla (a superphylum). The organisms have small genomes, and metabolic predictions indicate that their primary contributions to Earth’s biogeochemical cycles involve carbon and hydrogen metabolism, probably associated with symbiotic and/or fermentation-based lifestyles.
Conclusions: The results dramatically expand genomic sampling of the domain Archaea and clarify taxonomic designations within a major superphylum. This study, in combination with recently published work on bacterial phyla lacking cultivated representatives, reveals a fascinating phenomenon of major radiations of organisms with small genomes, novel proteome composition, and strong interdependence in both domains.
There is an increasing interest to combine phylogenetic data with distributional and ecological records to assess how natural communities arrange under an evolutionary perspective. In the microbial world there is also a need to go beyond the problematic species definition to deeply explore ecological patterns using genetic data. We explored links between evolution/phylogeny and community ecology using bacterial 16S rRNA gene information from a high altitude lakes district dataset. We described phylogenetic community composition, spatial distribution, and β-diversity and biogeographical patterns applying evolutionary relatedness without relying on any particular operational taxonomic unit definition. High altitude lakes districts usually contain a large mosaic of highly diverse small water bodies and conform a fine biogeographical model of spatially close but environmentally heterogeneous ecosystems. We sampled eighteen lakes in the Pyrenees with a selection criteria focused on capturing the maximum environmental variation within a small geographical area. The results showed highly diverse communities non-randomly distributed with phylogenetic β-diversity patterns mainly shaped by the environment and not by the spatial distance. Community similarity based on both bacterial taxonomic composition and phylogenetic β-diversity approach shared similar patterns and were primarily structured by similar environmental drivers. We observed a positive relationship between lake area and phylogenetic diversity with a slope consistent with highly dispersive planktonic organisms. The phylogenetic approach incorporated patterns of common ancestry into bacterial community analysis and emerged as a very convenient analytical tool for direct inter- and intrabiome biodiversity comparisons and sorting out microbial habitats with potential application in conservation studies for microorganisms. This article is protected by copyright. All rights reserved.
Identifying the traits that determine spatial distributions can be challenging when studying organisms, like bacteria, for which phenotypic information is limited or non-existent. However, genomic data provide another means to infer traits and determine the ecological attributes that account for differences in distributions. We determined the spatial distributions of ~124 000 soil bacterial taxa across a 3.41 km2 area to determine whether we could use phylogeny and/or genomic traits to explain differences in habitat breadth. We found that occupancy was strongly correlated with environmental range; taxa that were more ubiquitous were found across a broader range of soil conditions. Across the ~500 taxa for which genomic information was available, genomic traits were more useful than phylogeny alone in explaining the variation in habitat breadth; bacteria with larger genomes and more metabolic versatility were more likely to have larger environmental and geographical distributions. Just as trait-based approaches have proven to be so useful for understanding the distributions of animals and plants, we demonstrate that we can use genomic information to infer microbial traits that are difficult to measure directly and build trait-based predictions of the biogeographical patterns exhibited by microbes.
Amplified marker-gene sequences can be used to understand microbial community structure, but they suffer from a high level of sequencing and amplification artifacts. The UPARSE pipeline reports operational taxonomic unit (OTU) sequences with ≤1% incorrect bases in artificial microbial community tests, compared with >3% incorrect bases commonly reported by other methods. The improved accuracy results in far fewer OTUs, consistently closer to the expected number of species in a community.
Methanogen diversity and methanogenic potential in formation water obtained from the Minami-kanto gas field in Japan were investigated by using 16S rRNA gene libraries and culture-based enrichment methods, respectively. This region is the largest gas field that produces natural gases of dissolved-in-water type in Japan. Although the microbial population density was below statistical quantification limits (1 × 10 cells ml), autofluorescent coccoid and rod-shaped cells indicative of methanogens were observed. The represented genera in the archaeal 16S rRNA genes libraries were comprised of Methanobacterium, Methanospirillum, Methanocalculus, Methanococcus, Methanolobus and Methanosaeta. The dominant archaeal sequences were related to the hydrogenotrophic methanogens in the genus Methanobacterium. Of the methanogenic substrates tested using the formation water-based medium,H2-CO2 yielded the highest methane production. These results strongly suggest that the formation water of the Pleistocene strata in the gas fields harbor viable hydrogenotrophic methanogens and have possibly been making a contribution to ongoing methanogenesis.
Anaerobic treatment is an attractive option for the biological treatment of municipal wastewater. In this study, municipal wastewater was anaerobically treated with a bench-scale upflow anaerobic sludge blanket (UASB) reactor at temperatures from 6 to 31 °C for 18 months to investigate total chemical oxygen demand (COD) removal efficiency, archaeal community structure, and dissolved methane (D-CH(4)) recovery efficiency. The COD removal efficiency was more than 50% in summer and below 40% in winter with no evolution of biogas. Analysis of the archaeal community structures of the granular sludge from the UASB using 16S rRNA gene-cloning indicated that after microorganisms had adapted to low temperatures, the archaeal community had a lower diversity and the relative abundance of acetoclastic methanogens decreased together with an increase in hydrogenotrophic methanogens. D-CH(4), which was detected in the UASB effluent throughout the operation, could be collected with a degassing membrane. The ratio of the collection to recovery rates was 60% in summer and 100% in winter. For anaerobic treatment of municipal wastewater at lower temperatures, hydrogenotrophic methanogens play an important role in COD removal and D-CH(4) can be collected to reduce greenhouse gas emissions and avoid wastage of energy resources.
We report a long-term (i.e., 4.5 consecutive yr) monitoring of surface marine archaeal assemblages of the coastal Mediterranean Sea using quantitative polymerase chain reaction against specific phylogenetic and functional genes, and, for some specific samples, clone libraries of the 16S ribosomal ribonucleic acid gene. Archaea had a marked seasonal periodicity, with recurrent peaks of abundance in December and January and very low occurrence during summer, parallel to temporal changes in community composition. Group II.b Euryarchaeota sequences were mostly present during winter when water was nutrient-enriched, and phytoplankton were abundant. Group II.a sequences were, in turn, more abundant during summer when the water column is stratified, and nutrient concentrations and phytoplankton stocks were lower. Group I Crenarchaeota abundance was highest during winter and significantly correlated with that of archaeal ammonia monooxygenase (amoA) gene copies and nitrite concentrations, suggesting that Group I Crenarchaeota were ammonia oxidizers. The periodicity of archaeal assemblages matched the strong and predictable seasonality of the surface-water conditions in the northwestern Mediterranean Sea, and suggests a low degree of functional redundancy between archaeal groups. The distinct seasonal dynamics for Group II.a and II.b Euryarchaeota, and their close association with major ecosystem processes, indicate that they may play an important but as yet largely unknown role in the ocean.
Inhibition by light potentially influences the distribution of ammonia oxidizers in aquatic environments and is one explanation for nitrite maxima near the base of the euphotic zone of oceanic waters. Previous studies of photoinhibition have been restricted to bacterial ammonia oxidizers, rather than archaeal ammonia oxidizers, which dominate in marine environments. To compare the photoinhibition of bacterial and archaeal ammonia oxidizers, specific growth rates of two ammonia-oxidizing archaea (Nitrosopumilus maritimus and Nitrosotalea devanaterra) and bacteria (Nitrosomonas europaea and Nitrosospira multiformis) were determined at different light intensities under continuous illumination and light/dark cycles. All strains were inhibited by continuous illumination at the highest intensity (500 μE m(-2) s(-1)). At lower light intensities, archaeal growth was much more photosensitive than bacterial growth, with greater inhibition at 60 μE m(-2) s(-1) than at 15 μE m(-2) s(-1), where bacteria were unaffected. Archaeal ammonia oxidizers were also more sensitive to cycles of 8-h light/16-h darkness at two light intensities (60 and 15 μE m(-2) s(-1)) and, unlike bacterial strains, showed no evidence of recovery during dark phases. The findings provide evidence for niche differentiation in aquatic environments and reduce support for photoinhibition as an explanation of nitrite maxima in the ocean.
Although most hypotheses to explain the emergence of the eukaryotic lineage are conflicting, some consensus exists concerning the requirement of a genomic fusion between archaeal and bacterial components. Recent phylogenomic studies have provided support for eocyte-like scenarios in which the alleged 'archaeal parent' of the eukaryotic cell emerged from the Crenarchaeota/Thaumarchaeota. Here, we provide evidence for a scenario in which this archaeal parent emerged from within the 'TACK' superphylum that comprises the Thaumarchaeota, Crenarchaeota and Korarchaeota, as well as the recently proposed phylum 'Aigarchaeota'. In support of this view, functional and comparative genomics studies have unearthed an increasing number of features that are uniquely shared by the TACK superphylum and eukaryotes, including proteins involved in cytokinesis, membrane remodeling, cell shape determination and protein recycling.
Little more than 30 years since the discovery of the Archaea, over one hundred archaeal genome sequences are now publicly available, of which ∼40% have been released in the last two years. Their analysis provides an increasingly complex picture of archaeal phylogeny and evolution with the proposal of new major phyla, such as the Thaumarchaeota, and important information on the evolution of key central cellular features such as cell division. Insights have been gained into the events and processes in archaeal evolution, with a number of additional and unexpected links to the Eukaryotes revealed. Taken together, these results predict that many more surprises will be found as new archaeal genomes are sequenced.
Despite its widespread distribution and high levels of phylogenetic diversity, microbes are poorly understood creatures. We applied a phylogenetic ecology approach in the Kingdom Euryarchaeota (Archaea) to gain insight into the environmental distribution and evolutionary history of one of the most ubiquitous and largely unknown microbial groups. We compiled 16S rRNA gene sequences from our own sequence libraries and public genetic databases for two of the most widespread mesophilic Euryarchaeota clades, Lake Dagow Sediment (LDS) and Rice Cluster-V (RC-V). The inferred population history indicated that both groups have undergone specific nonrandom evolution within environments, with several noteworthy habitat transition events. Remarkably, the LDS and RC-V groups had enormous levels of genetic diversity when compared with other microbial groups, and proliferation of sequences within each single clade was accompanied by significant ecological differentiation. Additionally, the freshwater Euryarchaeota counterparts unexpectedly showed high phylogenetic diversity, possibly promoted by their environmental adaptability and the heterogeneous nature of freshwater ecosystems. The temporal phylogenetic diversification pattern of these freshwater Euryarchaeota was concentrated both in early times and recently, similarly to other much less diverse but deeply sampled archaeal groups, further stressing that their genetic diversity is a function of environment plasticity. For the vast majority of living beings on Earth (i.e. the uncultured microorganisms), how they differ in the genetic or physiological traits used to exploit the environmental resources is largely unknown. Inferring population history from 16S rRNA gene-based molecular phylogenies under an ecological perspective may shed light on the intriguing relationships between lineage, environment, evolution and diversity in the microbial world.
The distribution of archaeal amoA and 16S rRNA genes was evaluated in two marine-derived, meromictic lakes in the Canadian High Arctic: Lake A and Lake C1 on the northern coast of Ellesmere Island. The amoA gene was recorded in both lakes, with highest copy numbers in the oxycline. Sequence analysis showed that amoA from the two lakes shared 94% similarity, indicating at least two phylogenetically distinct clusters. Clone libraries of archaeal 16S rRNA genes from Lake A revealed strong vertical differences in archaeal community diversity and composition down the water column. The oxic layer was dominated by one group of Euryarchaeota affiliated to the Lake Dagow Sediment (LDS) cluster. This group was absent from the oxycline, which had an extremely low archaeal diversity of two phylotypes. Both belonged to the Crenarchaeota Marine Group I (MGI), the marine group that has been linked to archaeal amoA; however, there was a low ratio of amoA to MGI copy numbers, suggesting that many MGI Archaea did not carry the amoA gene. The anoxic zone contained representatives of the RC-V (Rice Cluster-V) and LDS clusters of Euryarchaeota. These results show the strong vertical differentiation of archaeal communities in polar meromictic lakes, and they suggest archaeal nitrification within the oxycline of these highly stratified waters.
The bacterioneuston (bacteria inhabiting the air-water interface) is poorly characterized and possibly forms a unique community in the aquatic environment. In high mountain lakes, the surface film is subjected to extreme conditions of life, suggesting the development of a specific and adapted bacterioneuston community. We have studied the surface film of a remote high mountain lake in the Pyrenees by cloning the PCR-amplified 16S rRNA gene and comparing with bacteria present in underlying waters (UW), and airborne bacteria from the dust deposited on the top of the snow pack. We did not detect unusual taxa in the neuston but rather very common and widespread bacterial groups. Betaproteobacteria and Actinobacteria accounted for >75% of the community composition. Other minor groups were Gammaproteobacteria (between 8% and 12%), Alphaproteobacteria (between 1% and 5%), and Firmicutes (1%). However, we observed segregated populations in neuston and UW for the different clades within each of the main phylogenetic groups. The soil bacterium Acinetobacter sp. was only detected in the snow-dust sample. Overall, higher similarities were found between bacterioneuston and airborne bacteria than between the former and bacterioplankton. The surface film in high mountain lakes appears as a direct interceptor of airborne bacteria useful for monitoring long-range bacterial dispersion.