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(a) Timeresolved absolute abundance of the Desulfosporosinus population (black circles) compared to all Bacteria and Archaea (gray triangles) in anoxic peat soil microcosms under various in situ-like conditions as determined by quantitative PCR (modified from reference 5). Error bars represent 1 standard deviation of the mean (n 3; n 2 for propionate with sulfate stimulation, all days, and butyrate with sulfate stimulation, day 50). (b) Corresponding overall transcriptional changes (mRNA of all CDS) of Desulfosporosinus sp. MAG SbF1 in the same anoxic microcosms. Error bars represent 1 standard deviation of the mean (n 3; n 2 for propionate with sulfate stimulation).
Source publication
The microbial rare biosphere represents the largest pool of biodiversity on Earth and constitutes, in sum of all its members, a considerable part of a habitat’s biomass. Dormancy or starvation is typically used to explain the persistence of low-abundance microorganisms in the environment. We show that a low-abundance microorganism can be highly tra...
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Context 1
... low-abundance Desulfosporosinus sp. MAG SbF1 represents an interesting case of the latter response type. When exposed to favorable, sulfate-reducing conditions in peat soil microcosms, the overall Desulfosporosinus population did not increase its population size of about 1.2 10 6 16S rRNA gene copies cm 3 soil (Fig. 2a) but strongly increased its cellular ribosome content by up to 1 order of magnitude (see Fig. S4 in the supplemental material) (5). In a preceding 16S rRNA (gene) amplicon study which analyzed the same microcosms, we could show that Desulfosporosinus OTU0051 is the major constituent of this Desulfosporosinus population (74% of all ...
Context 2
... rRNA copies of the overall Desulfosporosinus population (Fig. S4) (5) clearly corresponded to increased transcription of genes coding for ribosomal proteins in Desulfosporosinus sp. MAG SbF1 ( Fig. 3; Table S1a) (5). This cellular ribosome increase under sulfate-reducing conditions correlated well with an increase in all normalized mRNA counts (Fig. 2b). This is the first time that changes in population-wide 16S rRNA levels are proven to be directly linked to transcriptional activity for a rare biosphere ...
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Citations
... This is mainly due to the difficulty of recovering RNA from peat, because of high humic acid content inhibiting traditional nucleic acid extraction protocols and downstream analyses such as PCR amplification. No metatranscriptomic studies assessing changes in active functions after rewetting and compare to pristine peatlands were found in our literature search, but some have been carried out in natural peatlands (Lin et al. 2014;Hausmann et al. 2019). Additionally, other metatranscriptomic analyses have focused so far on Sphagnum associated microbiomes Stough et al. 2018;Dedysh and Ivanova 2019;Carrell et al. 2022a, b;Kolton et al. 2022), arctic peatlands (Tveit et al. 2013(Tveit et al. , 2014Belova et al. 2018;Dedysh and Ivanova 2019;Ziegelhofer and Kujala 2021;Bender et al. 2021) and specific microbial groups such as protists (Geisen et al. 2015) and Planctomycetes Ivanova et al. 2018;Dedysh and Ivanova 2019). ...
Restoration of drained peatlands through rewetting has recently emerged as a prevailing strategy to mitigate excessive greenhouse gas emissions and re-establish the vital carbon sequestration capacity of peatlands. Rewetting can help to restore vegetation communities and biodiversity, while still allowing for extensive agricultural management such as paludiculture. Belowground processes governing carbon fluxes and greenhouse gas dynamics are mediated by a complex network of microbial communities and processes. Our understanding of this complexity and its multi-factorial controls in rewetted peatlands is limited. Here, we summarize the research regarding the role of soil microbial communities and functions in driving carbon and nutrient cycling in rewetted peatlands including the use of molecular biology techniques in understanding biogeochemical processes linked to greenhouse gas fluxes. We emphasize that rapidly advancing molecular biology approaches, such as high-throughput sequencing, are powerful tools helping to elucidate the dynamics of key biogeochemical processes when combined with isotope tracing and greenhouse gas measuring techniques. Insights gained from the gathered studies can help inform efficient monitoring practices for rewetted peatlands and the development of climate-smart restoration and management strategies.
Supplementary Information
The online version contains supplementary material available at 10.1007/s10533-024-01122-6.
... On the other hand, sulfate-reducers (SRB) are unprecedentedly diversified taxonomically, with evaluated number of unique operational taxonomic units (OTU) exceeding tens of thousands (Vigneron et al., 2018). In some cases, SRB exhibits a unique natural behavior: they do not proliferate and maintain a low-density population, yet they remain transcriptomically and metabolically active (Hausmann et al., 2019). In that state, cells actively reduce sulfates and significantly influence their ecosystem, which led to the idea of SRB comprising rare biosphere. ...
Understanding the microbial communities involved in the global sulfur cycle is crucial for comprehending key biogeochemical processes on Earth. Most studies, however, are biased towards the marine ecosystems, as terrestrial sulfur cycle rarely investigated. In this study, we employed culture-dependent techniques and metagenomics to investigate functional, taxonomic and culturable of sulfur-cycling bacteria in extremely contaminated soils. Our findings reveal that elevated concentrations of xenobiotic pollutants, bulk sulfur content, and fluctuating redox conditions have shaped a unique microbial community involved in sulfur transformation. This community comprises non-canonical taxa carrying out typical reactions (e.g., sulfate-reducing acidobacteria), known taxa engaged in various oxidative, reductive, and organosulfur transformations (e.g., sulfur oxidizing alpha-, gamma-, and betaproteobacteria), as well as previously unidentified taxa that remain uncultured and may possess novel genes related to sulfur compound metabolism. Additionally, multiple taxa contribute to the replenishment of readily consumable compounds like sulfite and thiosulfate, facilitating cryptic biogeochemical cycling of molecules with high turnover rates but low absolute abundance. Our analysis also supports the idea that known sulfate-reducing bacteria behave differently in soils compared to aquatic habitats and belong to the soil rare biosphere, still greatly affecting their ecosystem.
... Desulfosporosinus species usually oxidize organic compounds incompletel y, ther eby pr oducing acetate (Alazard et al. 2010, Mayeux et al. 2013, Sánc hez-Andr ea et al. 2015, Vandieken et al. 2017 ). Howe v er, complete oxidation of propionate , lactate , and acetate to CO 2 by a Desulfosporosinus strain has been recently reported (Hausmann et al. 2019 ). On the other hand, as the bioreactor was fed with gl ycer ol, a w ell-kno wn substrate for acidotolerant Desulfosporosinus strains but also a substrate for Cellulomonas and Propionibacter aceae, competition for gl ycer ol ma y also ha v e occurr ed and limited the availability of organic carbon for SRB. ...
Arsenic (As) and antimony (Sb) from mining sites can seep into aquatic ecosystems by acid mine drainage (AMD). Here, the possibility of concomitantly removing As and Sb from acidic waters by precipitation of sulfides induced by sulfate-reducing bacteria (SRB) was investigated in a fixed-bed column bioreactor. The real AMD water used to feed the bioreactor contained nearly 1 mM As while the Sb concentrations were increased (0.008 ± 0.006 to 1.01 ± 0.07 mM) to obtain an Sb/As molar ratio = 1. Results showed that the addition of Sb did not affect the efficiency of As bio-precipitation. Sb was removed efficiently (up to 97.9% removal) between the inlet and outlet of the bioreactor, together with As (up to 99.3% removal) in all conditions. Sb was generally removed as it entered the bioreactor. Appreciable sulfate reduction occurred in the bioreactor, which could have been linked to the stable presence of a major SRB OTU affiliated with the Desulfosporosinus genus. The bacterial community included polymer degraders, fermenters, and acetate degraders. Results suggested that sulfate reduction could be a suitable bioremediation process for simultaneous removal of Sb and As from AMD.
... For example, the high activity of sulfate reduction was driven by the rare biosphere microorganism in a peatland (Pester et al., 2010). The rare biosphere bacteria played a predominant role in phenanthrene degradation (Sauret et al., 2014), as some low-abundance microorganisms can be highly transcriptionally active without growth (Hausmann et al., 2019). Thus, how to increase the activity of the rare species involved in straw decomposition is a significant issue for the acceleration of straw decomposition. ...
Bacteria is one of the most important drivers of straw degradation. However, the changes in bacterial community assemblage and straw-decomposing profiles during straw decomposition are not well understood. Based on cultivation-dependent and independent technologies, this study revealed that the “common species” greatly contributed to the dynamic variation of bacterial community during straw decomposition. Twenty-three functional strains involved in straw decomposition were isolated, but only seven were detected in the high-throughput sequencing data. The straw decomposers, including the isolated strains and the agents determined by functional prediction, constituted only 0.024% (on average) of the total bacterial community. The ecological network showed that most of the identified decomposers were self-existent without associations with other species. These results showed that during straw composition, community assembly might be greatly determined by the majority, but straw decomposition functions might be largely determined by the minority and emphasized the importance of the rare species in community-specific functions.
... Frontiers in Microbiology | www.frontiersin.org Cardenas et al., 2008;Lee et al., 2009;Madden et al., 2009;Senko et al., 2009;Ňancucheo and Johnson, 2014), and other low pH ecosystems such as peatlands (Hausmann et al., 2016(Hausmann et al., , 2019. Three moderately acidophilic or acidotolerant Desulfosporosinus species were isolated so far: Ds. acidiphilus (pH 3.6-5.5, ...
... Conceptually, rare microbes have low abundance, comprising usually less than 0.1% of the total community, although this exact value depends on the community (Jousset et al., 2017). Despite their relatively low abundance, the rare microbes are relevant to ecosystem functioning (Pascoal et al., 2021), contributing to several functions, such as nutrient cycling and biological control (Hausmann et al., 2019) and community stability (Jousset et al., 2017). Rare microbes are phylogenetically and functionally diverse (Yamamoto et al., 2019), representing a large reservoir of genetic traits of both known and potentially novel microbial functions (Elshahed et al., 2008;Lynch and Neufeld, 2015). ...
... Studies focusing on rare microbes assess the effect of distinct environments, from soil to marine ecosystems (Hamasaki et al., 2016;Hausmann et al., 2019). However, it is poorly understood the effect of potential pollutants, with high content of metal applied in the soil, on the dynamic of rare microbes. ...
Composted tannery sludge (CTS) promotes shifts in soil chemical properties, affecting microbial communities. Although the effect of CTS application on the bacterial community has been studied, it is unclear whether this impact discriminates between the dominant and rare species. This present study investigated how the dominant and rare bacterial communities respond over time to different concentrations of CTS application (0, 2.5, 5, 10, and 20 tons/ha) for 180 days. The richness of operational taxonomic units (OTU) was 30-fold higher in the rare than in the dominant biosphere. While some phyla shifted their relative abundance differently in the dominant and rare biosphere, some genera increased their relative abundance under higher CTS concentrations, such as Nocardioides (∼100%), Rubrobacter (∼300%), and Nordella (∼400%). Undominated processes largely governed the dominant biosphere (76.97%), followed by homogeneous (12.51%) and variable (8.03%) selection, and to a lesser extent, the dispersal limitation (2.48%). The rare biosphere was driven by the CTS application as evidenced by the exclusively homogeneous selection (100%). This study showed that the rare biosphere was more sensitive to changes in soil chemical parameters due to CTS application, which evidences the importance explore this portion of the bacterial community for its biotechnological use in contaminated soils.
... Ecological communities are generally composed of a few highly abundant species and numerous low abundance ones, which the latter is defined as the rare biosphere [1,2]. In microbiomes, rare microbial species potentially play crucial roles in ecosystem functioning, for instance, by preventing pathogen spread, controlling nutrient cycling, and contributing to pollutant degradation [3][4][5][6]. However, it remains unclear how distinct ecological processes interplay in determining the assembly and successional dynamics of the different types of microbial rarity. ...
Most ecological communities harbor many rare species (i.e., the rare biosphere), however, relatively little is known about how distinct ecological processes structure their existence. Here, we used spatiotemporal data on soil bacterial communities along a natural ecosystem gradient to model the relative influences of assembly processes structuring the rare and common biospheres. We found a greater influence of homogeneous selection (i.e., imposed by spatiotemporally constant variables) mediating the assembly of the rare biosphere, whereas the common biosphere was mostly governed by variable selection (i.e., imposed by spatial and/or temporal fluctuating variables). By partitioning the different types of rarity, we found homogeneous selection to explain the prevalence of permanently rare taxa, thus suggesting their persistence at low abundances to be restrained by physiological traits. Conversely, the dynamics of conditionally rare taxa were mostly structured by variable selection, which aligns with the ability of these taxa to switch between rarity and commonness as responses to environmental spatiotemporal variations. Taken together, our study contributes to the establishment of a link between conceptual and empirical developments in the ecology of the soil microbial rare biosphere. Besides, this study provides a framework to better understand, model, and predict the existence and dynamics of microbial rare biospheres across divergent systems and scales. ISME Communications; https://doi.
... Although we did not observe local peaks in relative abundance, the increase in RNA:DNA ratio and ratio variability as relative abundance decreases corroborates the idea that these taxa have higher sensitivity to changes in environmental conditions and habitat filtering. There is additional evidence of disproportional activity of the rare biosphere (15,30,35,36,55) and even transcriptionally active rare taxa that display no growth (56). Even if they did not peak in relative abundance, rare taxa seemed therefore to potentially play an important role in microbial processes given their high activity. ...
Bacterial community structure can change rapidly across short spatial and temporal scales as environmental conditions vary, but the mechanisms underlying those changes are still poorly understood. Here we assessed how a lake microbial community assembles by following its reorganization from the main tributary, which, when flowing into the lake, first traverses an extensive macrophyte-dominated vegetated habitat, before reaching the open water. Environmental conditions in the vegetated habitat changed drastically compared to both river and lake waters, and represented a strong environmental gradient for the incoming bacteria. We used amplicon sequencing of the 16S rRNA gene and transcript to reconstruct the shifts in relative abundance of individual taxa and link this to their pattern in activity (here assessed with RNA: DNA ratios). Our results indicate that major shifts in relative abundance were restricted mostly to rare taxa (<0.1% of relative abundance), which seemed more responsive to environmental changes. Dominant taxa (>1% of relative abundance), on the other hand, traversed the gradient mostly unchanged with relatively low and stable RNA: DNA ratios. We also identified a high level of local recruitment, and a seedbank of taxa capable of activating/inactivating, but these were almost exclusively associated with the rare biosphere. Our results suggest a scenario where the lake community results from a reshuffling of the rank abundance structure within the incoming rare biosphere, driven by selection and growth, and that numerical dominance is not a synonym of activity, growth rate or environmental selection, but rather reflect mass effects structuring these freshwater bacterial communities.
... Some rare taxa play crucial ecological functions in various biogeochemical processes and in human health [4]. For example, Pester and colleagues demonstrated that Desulfosporosinus, despite detected with a relative abundance of less than 0.006%, had a fundamental role in sulfate reduction in a peatland ecosystem [6], and maintained high cellular activities under in situ-like conditions in lab [7]. Bodelier and colleagues found that the rare methane-oxidizing bacteria play an unneglectable role in the dynamics and consumption of methane in a wetland [8]. ...
Background
Increasing studies have demonstrated potential disproportionate functional and ecological contributions of rare taxa in a microbial community. However, the study of the microbial rare biosphere is hampered by their inherent scarcity and the deficiency of currently available techniques. Sample-wise cross contaminations might be introduced by sample index misassignment in the most widely used metabarcoding amplicon sequencing approach. Although downstream bioinformatic quality control and clustering or denoising algorithms could remove sequencing errors and non-biological artifact reads, no algorithm could eliminate high quality reads from sample-wise cross contaminations introduced by index misassignment, making it difficult to distinguish between bona fide rare taxa and potential false positives in metabarcoding studies.
Results
We thoroughly evaluated the rate of index misassignment of the widely used NovaSeq 6000 and DNBSEQ-G400 sequencing platforms using both commercial and customized mock communities, and observed significant lower (0.08% vs. 5.68%) fraction of potential false positive reads for DNBSEQ-G400 as compared to NovaSeq 6000. Significant batch effects could be caused by stochastically introduced false positive or false negative rare taxa. These false detections could also lead to inflated alpha diversity of relatively simple microbial communities and underestimated that of complex ones. Further test using a set of cow rumen samples reported differential rare taxa by different sequencing platforms. Correlation analysis of the rare taxa detected by each sequencing platform demonstrated that the rare taxa identified by DNBSEQ-G400 platform had a much higher possibility to be correlated with the physiochemical properties of rumen fluid as compared to NovaSeq 6000 platform. Community assembly mechanism and microbial network correlation analysis indicated that false positive or negative rare taxa detection could lead to biased community assembly mechanism and identification of fake keystone species of the community.
Conclusions
We highly suggest proper positive/negative/blank controls, technical replicate settings, and proper sequencing platform selection in future amplicon studies, especially when the microbial rare biosphere would be focused.
... Although low abundance could mean low contribution to biogeochemical cycling, contribution to sulfur and carbon, and even iron cycling (Neal et al. 2001) by Desulfosporosinus spp. has recently been reported (Hausmann et al. 2019). ...
We investigated the microbial community composition in three different mine tunnels from Hualgayoc (Cajamarca, Peru) and the metabolic activity of acidophilic sulfate-reducing bacteria (aSRB) enriched from acidic sediments of the mining tunnels. Microbial community composition in environmental samples was analyzed by 16S rRNA amplicon sequencing. Metallibacterium and Acidiphilium were found as the most abundant bacteria in PM1 and PM2 sites, respectively, while Cyanobacteria was abundant in PM3 site. Isosphaera and Pseudomonas thrived in the acidic water of PM2 site as well. Sulfate reduction at low pH was then evaluated in microcosm experiments showing activity even at pH 3.4. Hydrogen was the most favorable electron donor in terms of sulfate reducing rates (0.5 mM day−1 at pH 5.1) and sulfide production (4.9 mM at the end of the experiment). Sequences affiliated to Desulfosporosinus and Desulfovibrio were abundant in the hydrogen microcosms (60.3 and 17.8%, respectively). These sequences were not detected in sediments, but their occurrence in the microcosms suggests their low abundance in the studied AMD systems. Our results expand the phyla detected in AMD environments and contribute to the understanding of aSRB for the possibility of applying these microorganisms in bioremediation.
