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Unicellular organisms dominate the eukaryotic lineages. A schematic diagram of the eukaryotic tree of life showing the major groups (Dorrell & Smith (2011); Burki 2014). At present the positions of the Haptophytes, Telonemids, Cryptomonads and Centrohelids remain uncertain (Incertae sedis). Multicellularity has evolved only seven times (highlighted with filled circles); all other lineages are essentially microbial.
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Extensive sampling and metagenomics analyses of plankton communities across all aquatic environments are beginning to provide insights into the ecology of microbial communities. In particular the importance of metabolic exchanges that provide a foundation for ecological interactions between microorganisms has emerged as a key factor in forging the...
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... are the 'unseen majority' of life on Earth. As well as being numerically dominant, they also constitute the major phylogenetic diversity, even within the Eukaryotes where nearly every lineage is dominated by unicellular or microscopic species, and where multicellularity is the excep- tion rather than the rule (Fig. 1). Moreover, in a range of ecosystems including the soil and ocean biomes, microorgan- isms make the major impact on global processes such as the biogeochemical cycling of carbon, nitrogen and sulphur (Falkowski et al. 2008;van der Heijden et al. 2008). They are par- ticularly important in the aquatic environment because here a subset of ...
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Background: Understanding microbial interactions in engineering bioprocesses is important to enhance and optimize performance outcomes and requires dissection of the multi-layer complexities of microbial communities. However, unraveling microbial interactions as well as substrates involved in complex microbial communities is a challenging task. Her...
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... The interconnected evolutionary history of cyanobacteria and bacteria allows the formation of various complex interactions between cyanobacteria and heterotrophic bacteria, like trophallaxis, signals transduction, and transgenosis (Kouzuma and Watanabe 2015). Metagenomes, metaproteomes, and metatranscriptomes are the main ways to illustrate the interactions of phytoplankton and heterotrophic bacteria, and these methods can confirm many species existing in the environment and provide the holistic metabolic abilities of the community studied (Kazamia et al. 2016). Few of these studies were done in axenic conditions, which resulted in most of these interaction features (Grossart and Simon 2007) and bacterial ecological functions ) unknown, especially the exact interactions of these microbes (Zhu et al. 2019). ...
... Few of these studies were done in axenic conditions, which resulted in most of these interaction features (Grossart and Simon 2007) and bacterial ecological functions ) unknown, especially the exact interactions of these microbes (Zhu et al. 2019). Co-cultures of cyanobacteria and specific bacteria wellcharacterized under laboratory conditions are offering the foundation to develop ecological principles that represent the microbial community dynamics and lifestyle, and can reveal the specific interactions at the cellular and molecular levels (Kazamia et al. 2016). Therefore, only combined with the defined co-cultures in the laboratory, transcriptomic, metagenomic, and metabolomic approaches can deepen our cognition on these interactions preferably. ...
An alpha-proteobacterial strain JXJ CY 53 T was isolated from the cyanosphere of Microcystis sp. FACHB-905 (MF-905) collected from Lake Dianchi, China. JXJ CY 53 T was observed to be an aerobic, Gram-stain-negative, oval shaped, and mucus-secreting bacterium. It had C18:1ω7c and C16:0 as the major cellular fatty acids, Q-10 as the predominant ubiquinone, and sphingoglycolipid, diphosphatidylglycerol, phosphatidylcholine, and phosphatidylmethylethanolamine as the polar lipids. The G + C content of DNA was 65.85%. The bacterium had 16S rRNA gene sequence identities of 98.9% and 98.7% with Sphingomonas panni DSM 15761 T and Sphingomonas hankookensis KCTC 22579 T, respectively, while less than 97.4% identities with other members of the genus. Further taxonomic analysis indicated that JXJ CY 53 T represented a new member of Sphingomonas, and the species epithet was proposed as Sphingomonas lacusdianchii sp. nov. (type strain JXJ CY 53 T = KCTC 72813 T = CGMCC 1.17657 T). JXJ CY 53 T promoted the growth of MF-905 by providing bio-available phosphorus and nitrogen, plant hormones, vitamins, and carotenoids. It could modulate the relative abundances of nonculturable bacteria associated with MF-905 and influence the interactions of MF-905 and other bacteria isolated from the cyanobacterium, in addition to microcystin production characteristics. Meanwhile, MF-905 could provide JXJ CY 53 T dissolved organic carbon for growth, and control the growth of JXJ CY 53 T by secreting specific chemicals other than microcystins. Overall, these results suggest that the interactions between Microcystis and its attached bacteria are complex and dynamic, and may influence the growth characteristics of the cyanobacterium. This study provided new ideas to understand the interactions between Microcystis and its attached bacteria.
Key points
• A novel bacterium (JXJCY 53T) was isolated from the cyanosphere of Microcystis sp. FACHB-905 (MF-905)
• JXJCY 53Tmodulated the growth and microcystin production of MF-905
• MF-905 could control the attached bacteria by specific chemicals other than microcystins (MCs)
... Yet, the interactions between cyanobacteria and heterotrophs can be far more complex since they might change over time [45] or under different culture conditions [53]. The mutualism might also occur beyond the two-species framework [55], which makes it even more challenging to understand the processes among multiple organisms. ...
Background Picocyanobacteria from the genera Prochlorococcus, Synechococcus, and Cyanobium are the most widespread photosynthetic organisms in aquatic ecosystems. However, their freshwater populations remain poorly explored, due to uneven and insufficient sampling across diverse inland waterbodies.
Results In this study, we present 170 high-quality genomes of freshwater picocyanobacteria from non-axenic cultures collected across Central Europe. In addition, we recovered 33 genomes of their potential symbiotic partners affiliated with four genera, Pseudomonas, Mesorhizobium, Acidovorax, and Hydrogenophaga. The genomic basis of symbiotic interactions involved heterotrophs benefiting from picocyanobacteria-derived nutrients while providing detoxification of ROS. The global abundance patterns of picocyanobacteriarevealed ecologically significant ecotypes, associated with trophic status, temperature, and pH as key environmental factors. The adaptation of picocyanobacteria in (hyper-)eutrophic waterbodies could be attributed to their colonial lifestyles and CRISPR-Cas systems. The prevailing CRISPR-Cas subtypes in picocyanobacteria were I-G and I-E, which appear to have been acquired through horizontal gene transfer from other bacterial phyla.
Conclusions Our findings provide novel insights into the population diversity, ecology, and evolutionary strategies of the most widespread photoautotrophs within freshwater ecosystems.
... The analysis of metagenomes, metatranscriptomes and metaproteomes on natural water bloom samples play important roles in the recognition of interactions in phytoplankton communities (Kazamia et al., 2016). However, these technologies can only let us know the overall metabolic capability and ecological state of a community (Kazamia et al., 2016), and many aspects of these interactions, especially specific interactions of the microbes within, are still unknown (Grossart and Simon, 2007;Kazamia et al., 2016;Zhang et al., 2019) because of most of these studies were performed under non-axenic conditions (Grossart and Simon, 2007;Zhang et al., 2019). ...
... The analysis of metagenomes, metatranscriptomes and metaproteomes on natural water bloom samples play important roles in the recognition of interactions in phytoplankton communities (Kazamia et al., 2016). However, these technologies can only let us know the overall metabolic capability and ecological state of a community (Kazamia et al., 2016), and many aspects of these interactions, especially specific interactions of the microbes within, are still unknown (Grossart and Simon, 2007;Kazamia et al., 2016;Zhang et al., 2019) because of most of these studies were performed under non-axenic conditions (Grossart and Simon, 2007;Zhang et al., 2019). Specific interactions can only probably be understood through physiological experiments using defined systems such as co-cultures of known and well-characterized partners in the laboratory, which can shed light on the interactions at the molecular and cellular levels (Kazamia et al., 2016). ...
... The analysis of metagenomes, metatranscriptomes and metaproteomes on natural water bloom samples play important roles in the recognition of interactions in phytoplankton communities (Kazamia et al., 2016). However, these technologies can only let us know the overall metabolic capability and ecological state of a community (Kazamia et al., 2016), and many aspects of these interactions, especially specific interactions of the microbes within, are still unknown (Grossart and Simon, 2007;Kazamia et al., 2016;Zhang et al., 2019) because of most of these studies were performed under non-axenic conditions (Grossart and Simon, 2007;Zhang et al., 2019). Specific interactions can only probably be understood through physiological experiments using defined systems such as co-cultures of known and well-characterized partners in the laboratory, which can shed light on the interactions at the molecular and cellular levels (Kazamia et al., 2016). ...
Harmful algal blooms (HABs) in natural waters are of escalating global concern due to their detrimental impact on environmental health. Emerging evidence indicates that algae-bacteria symbionts can affect HAB features, though much about this interplay remains largely unexplored. The current study isolated a new species of Mucilaginibacter (type strain JXJ CY 39T) from culture biomass of the bloom-causing Microcystis aeruginosa FACHB-905 (Maf) from Lake Dianchi, China. Strain JXJ CY 39T was an aerobic, Gram-stain-negative rod bacterium that grew at 5–38°C, pH 4.0–11.0, and 0–3.0% NaCl. Taxonomic evaluation proposed a new species, with Mucilaginibacter lacusdianchii sp. nov., as the species epithet. Experimental results revealed that strain JXJ CY 39T spurred the growth of Maf by supplying soluble phosphorus and nitrogen during cultivation, despite the unavailability of soluble phosphorus and nitrogen. Additionally, by producing the plant hormone indole-3-acetate, strain JXJ CY 39T possibly impacted Maf’s functionality. Results from co-culture experiments with other strains from Maf biomass showed possible effects of strain JXJ CY 39T on the relationship between Maf and other cohabiting bacteria, as well as microcystin toxin production characteristics. Although Maf could foster the growth of strain JXJ CY 39T by supplying organic carbon, the strain’s growth could be regulated via specific chemical compounds based on antibiotic assays. Community composition analysis disclosed that this Mucilaginibacter strain positively affected Maf’s growth and modified densities and types of bacteria linked to Maf. Overall, these results suggest that the interactions between important HAB-causing organisms and their attached bacteria are complex, dynamic, and may influence the growth characteristics of algae.
... Following application, diffuse inputs of herbicides to non-target areas occur unavoidably (Chow et al., 2020;de Souza et al., 2020;Mohaupt et al., 2020;Ulrich, Pfannerstill, et al., 2021), and herbicides can exert adverse effects on non-target organisms such as crustaceans, fish and algae (De Brito Rodrigues et al., 2017;Spycher et al., 2018;Wijewardene, Wu, Qu, et al., 2021). On a community level, macrophytes, phytoplankton and bacteria form metaorganism-like synergies by mutual nutrient supply (Kazamia et al., 2016), hence, shifts in macrophytes due to herbicide contamination may be followed by microbiome changes. Looking at the direct effects of herbicides on aquatic bacterial communities, the current database is more than limited. ...
Herbicides are important, ubiquitous environmental contaminants, but little is known about their interaction with bacterial aquatic communities. Here, we sampled a protected natural freshwater habitat and characterised its microbiome in interaction with herbicides. We evolved the freshwater microbiomes in a microcosm assay of exposure (28 days) to flufenacet and metazachlor at environmental concentrations of 0.5, 5 and 50 μg L ⁻¹ . Inhibitory effects of herbicides were exemplarily assessed in cultured bacteria from the same pond ( Pseudomonas alcaligenes , Paenibacillus amylolyticus and Microbacterium hominis ). Findings were compared to long‐term concentrations as provided by local authorities. Here, environmental concentrations reached up to 11 μg L ⁻¹ (flufenacet) and 76 μg L ⁻¹ (metazachlor). Bacteria were inhibited at minimum inhibitory concentrations far above these values; however, concentrations of 50 μg L ⁻¹ of flufenacet resulted in measurable growth impairment. While most herbicide‐exposed microcosm assays did not differ from controls, Acidobacteria were selected at high environmental concentrations of herbicides. Alpha‐diversity (e.g., taxonomic richness on phylum level) was reduced when aquatic microbiomes were exposed to 50 μg metazachlor or flufenacet. One environmental strain of P. alcaligenes showed resistance to high concentrations of flufenacet (50 g L ⁻¹ ). In total, this study reveals that ecologic imbalance due to herbicide use significantly impacts aquatic microbiomes.
... Interactions between diatoms and bacteria are some of the most important relationships in aquatic environments [3][4][5]. These interactions are diverse and complex and can result in mutualistic, commensal, competitive, and antagonistic interactions that can lead to the demise or success of interacting species [5][6][7]. Although the precise characteristics of these interactions may exhibit variability, chemical compounds emerge as the main drivers of these dynamics [8][9][10]. ...
Diatoms are responsible for the fixation of ca. 20% of the global CO2 and live associated with bacteria that utilize the organic substances produced by them. Current research trends in marine microbial ecology show which diatom and bacteria interact mediated through the production and exchange of infochemicals. Polyunsaturated aldehydes (PUA) are organic molecules released by diatoms that are considered to have infochemical properties. In this work, we investigated the possible role of PUA as a mediator in diatom–bacteria interactions. To this end, we compare the PUA profile of a newly isolated oceanic PUA producer diatom, Cyclotella cryptica, co-cultured with and without associated bacteria at two phosphate availability conditions. We found that the PUA profile of C. criptica cultured axenically was different than its profile when it was co-cultured with autochthonous (naturally associated) and non-autochthonous bacteria (unnaturally inoculated). We also observed that bacterial presence significantly enhanced diatom growth and that C. cryptica modulated the percentage of released PUA in response to the presence of bacteria, also depending on the consortium type. Based on our results, we propose that this diatom could use released PUA as a specific organic matter sign to attract beneficial bacteria for constructing its own phycosphere, for more beneficial growth.
... We hypothesize that this dynamic shift in 2-methylhopanoid producers and the rise of algae proceeded in concert. It is well known that eukaryotes depend on symbiotic microbes for nutrient acquisition and have co-evolved with those symbionts, as observed for algae, plants and animals 38,39 . For instance, eukaryotes cannot biosynthesize vitamin B 12 (cobalamin) de novo, although the majority of green algae require this nutrient for the biosynthesis of the essential amino acid methionine (Supplementary Note9) 40 . ...
Fossilized lipids offer a rare glimpse into ancient ecosystems. 2-Methylhopanes in sedimentary rocks were once used to infer the importance of cyanobacteria as primary producers throughout geological history. However, the discovery of hopanoid C-2 methyltransferase (HpnP) in Alphaproteobacteria led to the downfall of this molecular proxy. In the present study, we re-examined the distribution of HpnP in a new phylogenetic framework including recently proposed candidate phyla and re-interpreted a revised geological record of 2-methylhopanes based on contamination-free samples. We show that HpnP was probably present in the last common ancestor of cyanobacteria, while the gene appeared in Alphaproteobacteria only around 750 million years ago (Ma). A subsequent rise of sedimentary 2-methylhopanes around 600 Ma probably reflects the expansion of Alphaproteobacteria that coincided with the rise of eukaryotic algae—possibly connected by algal dependency on microbially produced vitamin B 12 . Our findings re-establish 2-methylhopanes as cyanobacterial biomarkers before 750 Ma and thus as a potential tool to measure the importance of oxygenic cyanobacteria as primary producers on early Earth. Our study illustrates how genetics can improve the diagnostic value of biomarkers and refine the reconstruction of early ecosystems.
... Genome sequence analysis has revealed that the majority of the sequenced microorganisms are auxotrophic, relying on other members of the communities to acquire necessary amino acids or vitamins 14 . B-vitamins are public goods in oceanic plankton communities 15 . Eukaryotic algae are frequently found to be vitamin B auxotrophs 16 , and they form mutualistic relationships with vitaminsupplying bacteria 17 . ...
Public metabolites such as vitamins play critical roles in maintaining the ecological functions of microbial community. However, the biochemical and physiological bases for fine-tuning of public metabolites in the microbiome remain poorly understood. Here, we examine the interactions between myxobacteria and Phytophthora sojae , an oomycete pathogen of soybean. We find that host plant and soil microbes complement P. sojae’ s auxotrophy for thiamine. Whereas, myxobacteria inhibits Phytophthora growth by a thiaminase I CcThi1 secreted into extracellular environment via outer membrane vesicles (OMVs). CcThi1 scavenges the required thiamine and thus arrests the thiamine sharing behavior of P. sojae from the supplier, which interferes with amino acid metabolism and expression of pathogenic effectors, probably leading to impairment of P. sojae growth and pathogenicity. Moreover, myxobacteria and CcThi1 are highly effective in regulating the thiamine levels in soil, which is correlated with the incidence of soybean Phytophthora root rot. Our findings unravel a novel ecological tactic employed by myxobacteria to maintain the interspecific equilibrium in soil microbial community.
... Compounds released by bacteria and known to be reincorporated by photoautotrophs for biomass include ammonium 5 , amino acids 13 , and carbon dioxide 14 . However, nutrient remineralization has not been identified as a primary mechanism of algal growth promotion by bacteria 15 , perhaps because in nature, they are often decoupled in time and space 16 . Nonetheless, since different bacteria are known to consume different sources of organic matter, it seems plausible that different bacteria likewise express different rates of nutrient remineralization. ...
... Considering these possibilities, we tested which of the 15 algalassociated strains incorporated small polar molecules with nitrate as the N source, using simultaneously added 13 C-labeled glycolate and 15 N-labeled nitrate. We chose glycolate over glucose since algal biofuel production ponds are super-saturated with oxygen during the day that lead to glycolate production via photorespiration 28 . ...
Bacterial remineralization of algal organic matter fuels algal growth but is rarely quantified. Consequently, we cannot currently predict whether some bacterial taxa may provide more remineralized nutrients to algae than others. Here, we quantified bacterial incorporation of algal-derived complex dissolved organic carbon and nitrogen and algal incorporation of remineralized carbon and nitrogen in fifteen bacterial co-cultures growing with the diatom Phaeodactylum tricornutum at the single-cell level using isotope tracing and nanoSIMS. We found unexpected strain-to-strain and cell-to-cell variability in net carbon and nitrogen incorporation, including non-ubiquitous complex organic nitrogen utilization and remineralization. We used these data to identify three distinct functional guilds of metabolic interactions, which we termed macromolecule remineralizers, macromolecule users, and small-molecule users, the latter exhibiting efficient growth under low carbon availability. The functional guilds were not linked to phylogeny and could not be elucidated strictly from metabolic capacity as predicted by comparative genomics, highlighting the need for direct activity-based measurements in ecological studies of microbial metabolic interactions.
... 11,12 Within aquatic systems, phytoplankton serves as the dominant primary producer and contributes almost 50% of global photosynthesis. 13 Algae with a planktonic nature have to directly face a variety of antibiotic challenges. The majority of current knowledge is regarding the acute toxicity of antibiotics to the single algae species, such as the strong inhibition effects of 40 μg L −1 erythromycin and 20 mg L −1 florfenicol on Isochrysis galbana and Microcystis f los-aquae, respectively. ...
... The possible explanation is based on the fact that natural waters cover highly various microbial communities, most of which could directly or indirectly function to modulate the algae nutrition, growth, and health. 13,43 In the natural environment, algae inevitably suffer from various biotic/abiotic stress, making the recruitment process essential and deserving of attention. 44 These findings emphasize besides genetic factor on the bacterial assemblage 45 that exogenous stress-induced recruitment of specific algaeassociated microbiome is also a non-negligible effective mechanism. ...
... 29 The aforementioned bacterial structure shift induced by antibiotics in turn facilitates the functions related to the algae development such as the metabolism of cofactors and vitamins, glycan biosynthesis and metabolism, metabolism of terpenoids and polyketides, transport, and catabolism, while decreases the functions related to normal physiological metabolism. 13,20,40 Taken as a whole, these findings highlight that when challenged by antibiotics, algae could employ a specific strategy to recruit beneficial bacteria to cope with antibiotic stress. ...
Insights into the symbiotic relation between eukaryotic hosts and their microbiome lift the curtain on the crucial roles of microbes in host fitness, behavior, and ecology. However, it remains unclear whether and how abiotic stress shapes the microbiome and further affects host adaptability. This study first investigated the effect of antibiotic exposure on behavior across varying algae taxa at the community level. Chlorophyta, in particular Chlorella vulgaris, exhibited remarkable adaptability to antibiotic stress, leading to their dominance in phytoplankton communities. Accordingly, we isolated C. vulgaris strains and compared the growth of axenic and nonaxenic ones under antibiotic conditions. The positive roles of antibiotics in algal growth were apparent only in the presence of bacteria. Results of 16S rRNA sequencing further revealed that antibiotic challenges resulted in the recruitment of specific bacterial consortia in the phycosphere, whose functions were tightly linked to the host growth promotion and adaptability enhancement. In addition, the algal phycosphere was characterized with 47-fold higher enrichment capability of antibiotic resistance genes (ARGs) than the surrounding water. Under antibiotic stress, specific ARG profiles were recruited in C. vulgaris phycosphere, presumably driven by the specific assembly of bacterial consortia and mobile genetic elements induced by antibiotics. Moreover, the antibiotics even enhanced the dissemination potential of the bacteria carrying ARGs from the algal phycosphere to broader environmental niches. Overall, this study provides an in-depth understanding into the potential functional significance of antibiotic-mediated recruitment of specific algae-associated bacteria for algae adaptability and ARG proliferation in antibiotic-polluted waters.
... Microbial interactions are critical to microbiome composition and functions, which have broad ecological implications and important biotechnological applications [1,2]. Recent developments in metagenomics have advanced our understanding of microbial interactions under environmental stress and shed light on the ecological drivers of microbial interactions [3][4][5]. Phages, known as prokaryotic viruses, are an important component of microbial assemblies [6]. Phages can affect microbial community through multiple patterns (e.g., cell lysis and horizontal gene transfer) [7]. ...
Prokaryotic antiviral systems are important mediators for prokaryote-phage interactions, which have significant implications for the survival of prokaryotic community. However, the prokaryotic antiviral systems under environmental stress are poorly understood, limiting the understanding of microbial adaptability. Here, we systematically investigated the profile of the prokaryotic antiviral systems at the community level and prokaryote-phage interactions in the drinking water microbiome. Chlorine disinfectant was revealed as the main ecological driver for the difference in prokaryotic antiviral systems and prokaryote-phage interactions. Specifically, the prokaryotic antiviral systems in the microbiome exhibited a higher abundance, broader antiviral spectrum, and lower metabolic burden under disinfectant stress. Moreover, significant positive correlations were observed between phage lysogenicity and enrichment of antiviral systems (e.g., Type IIG and IV restriction-modification (RM) systems, and Type II CRISPR-Cas system) in the presence of disinfection, indicating these antiviral systems might be more compatible with lysogenic phages and prophages. Accordingly, there was a stronger prokaryote-phage symbiosis in disinfected microbiome, and the symbiotic phages carried more auxiliary metabolic genes (AMGs) related to prokaryotic adaptability as well as antiviral systems, which might further enhance prokaryote survival in drinking water distribution systems. Overall, this study demonstrates that the prokaryotic antiviral systems had a close association with their symbiotic phages, which provides novel insights into prokaryote-phage interactions and microbial environmental adaptation.
