Pangenomics reveal diversification of enzyme families and niche specialization in globally abundant SAR202 bacteria

Saw, Jimmy H.; Nunoura, Takuro; Hirai, Miho; Takaki, Yoshihiro; Parsons, Rachel; Michelsen, Michelle L.; Longnecker, Krista; Kujawinski, Elizabeth B.; Stepanauskas, Ramūnas; Landry, Zachary C.; Carlson, Craig A.; Giovannoni, Stephen J.

doi:10.1101/692848

Cited by 4 publications

(7 citation statements)

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“…In fact, SAR202 have been reported to have diverse metabolic pathways that may link the biogeochemical cycles of carbon, nitrogen, and sulfur ( Thrash et al, 2017 ; Colatriano et al, 2018 ; Mehrshad et al, 2018a ). SAR202 lineages were also reported to develop specialized metabolism to oxidize different groups of recalcitrant organic compounds, via expansion of different combinations of paralogous genes ( Landry et al, 2017 ; Saw et al, 2019 ). The diversified metabolisms and capability to degrade various groups of recalcitrant organic matter would allow SAR202 to adapt different niches, linking different biogeochemical reactions, and could be a possible reason for the important role of SAR202 clade in maintaining network structure and mediating interactions in prokaryotic communities in the sediment of hadal trenches.…”

Section: Discussionmentioning

confidence: 99%

Bulk and Active Sediment Prokaryotic Communities in the Mariana and Mussau Trenches

Liu

Wang

et al. 2020

Front. Microbiol.

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Surprisingly high rates of microbial respiration have recently been reported in hadal trench sediment, yet the potentially active microorganisms and specific microbe–microbe relationships in trench sediment are largely unknown. We investigated the bulk and active prokaryotic communities and co-occurrence interactions of different lineages in vertically sectioned sediment cores taken from the deepest points of the Mariana and Mussau Trenches. Analysis on species novelty revealed for the first time the high rate of novel lineages in the microbial communities of the hadal trenches. Using 95, 97, and 99% similarity as thresholds, averagely 22.29, 32.3, and 64.1% of total OTUs retrieved from sediments of the two trenches were identified as the potentially novel lineages, respectively. The compositions of the potentially active communities, revealed via ribosomal RNA (rRNA), were significantly different from those of bulk communities (rDNA) in all samples from both trenches. The dominant taxa in bulk communities generally accounted for low proportions in the rRNA libraries, signifying that the abundance was not necessarily related to community functions in the hadal sediments. The potentially active communities showed high diversity and composed primarily of heterotrophic lineages, supporting their potential contributions in organic carbon consumption. Network analysis revealed high modularity and non-random co-occurrence of phylogenetically unrelated taxa, indicating highly specified micro-niches and close microbial interactions in the hadal sediments tested. Combined analysis of activity potentials and network keystone scores revealed significance of phyla Chloroflexi and Gemmatimonadetes, as well as several potentially alkane-degrading taxa in maintaining microbial interactions and functions of the trench communities. Overall, our results demonstrate that the hadal trenches harbor diverse, closely interacting, and active microorganisms, despite the extreme environmental conditions.

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Section: Discussionmentioning

confidence: 99%

Bulk and Active Sediment Prokaryotic Communities in the Mariana and Mussau Trenches

Liu

Wang

et al. 2020

Front. Microbiol.

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“…Our remineralization experiments demonstrate that prokaryotic cell densities increased by approximately fourfold over 5 days when a natural prokaryotic community from 200 m was mixed with filtrate enriched with zooplankton excreta (Figure 3A). Over this same period the bacterioplankton community structure in all treatments shifted significantly (SIMPROF and Pearson Correlation; p < 0.05) from mesopelagic lineages such as SAR11deep and SAR202 clades, members of which specialize in the metabolism of more recalcitrant DOM (Carlson et al, 2009;Liu et al, 2020;Saw et al, 2020), to larger copiotrophic groups including Alteromonadales, Pseudoalteromonadaceae, Rhodobacterales, and Flavobacteriales. The increase in the relative contribution of Alteromonadales lineages (specifically Marinobacter and Alteromonas) to total 16S rRNA amplicons was ubiquitous across the control, carryover, and copepod treatments.…”

Section: B10)mentioning

confidence: 94%

“…By the time ambient organic matter produced in the surface reaches the mesopelagic, the most labile fractions have been consumed, leaving behind compounds that have resisted or escaped rapid degradation by the epipelagic microbial community (the recalcitrant fraction; Carlson, 2002;Hansell, 2013). Thus, many mesopelagic prokaryotes are specialized to use this degraded organic matter (Giovannoni and Stingl, 2005;Morris et al, 2005;Landry et al, 2017;Saw et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Migratory Zooplankton Excreta and Its Influence on Prokaryotic Communities

et al. 2020

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Particulate organic matter (POM) (fecal pellets) from zooplankton has been demonstrated to be an important nutrient source for the pelagic prokaryotic community. Significantly less is known about the chemical composition of the dissolved organic matter (DOM) produced by these eukaryotes and its influence on pelagic ecosystem structure. Zooplankton migrators, which daily transport surface-derived compounds to depth, may act as important vectors of limiting nutrients for mesopelagic microbial communities. In this role, zooplankton may increase the DOM remineralization rate by heterotrophic prokaryotes through the creation of nutrient rich “hot spots” that could potentially increase niche diversity. To explore these interactions, we collected the migratory copepod Pleuromamma xiphias from the northwestern Sargasso Sea and sampled its excreta after 12–16 h of incubation. We measured bulk dissolved organic carbon (DOC), dissolved free amino acids (DFAA) via high performance liquid chromatography and dissolved targeted metabolites via quantitative mass spectrometry (UPLC-ESI-MSMS) to quantify organic zooplankton excreta production and characterize its composition. We observed production of labile DOM, including amino acids, vitamins, and nucleosides. Additionally, we harvested a portion of the excreta and subsequently used it as the growth medium for mesopelagic (200 m) bacterioplankton dilution cultures. In zooplankton excreta treatments we observed a four-fold increase in bacterioplankton cell densities that reached stationary growth phase after five days of dark incubation. Analyses of 16S rRNA gene amplicons suggested a shift from oligotrophs typical of open ocean and mesopelagic prokaryotic communities to more copiotrophic bacterial lineages in the presence of zooplankton excreta. These results support the hypothesis that zooplankton and prokaryotes are engaged in complex and indirect ecological interactions, broadening our understanding of the microbial loop.

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“…The cell abundances presented here indicate that their increasing proportional abundance at depth is due to stronger decrease in the cell abundances of other groups (Figure 4 and Supplementary Table 3). Very little is currently known about these two taxonomic groups, but previous genetic observations suggest that they possess distinct metabolic capabilities, and may be involved in the degradation of recalcitrant organic matter (SAR202 clade; Landry et al, 2017;Colatriano et al, 2018;Saw et al, 2019), or, in sulfur oxidation (SAR324 clade; Swan et al, 2011;Sheik et al, 2014).…”

Section: Enigmatic Microbial Lineages Increase In Cell Abundance Toward the Deep Oceanmentioning

confidence: 99%

Spatial Distribution of Arctic Bacterioplankton Abundance Is Linked to Distinct Water Masses and Summertime Phytoplankton Bloom Dynamics (Fram Strait, 79°N)

et al. 2021

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The Arctic is impacted by climate warming faster than any other oceanic region on Earth. Assessing the baseline of microbial communities in this rapidly changing ecosystem is vital for understanding the implications of ocean warming and sea ice retreat on ecosystem functioning. Using CARD-FISH and semi-automated counting, we quantified 14 ecologically relevant taxonomic groups of bacterioplankton (Bacteria and Archaea) from surface (0–30 m) down to deep waters (2,500 m) in summer ice-covered and ice-free regions of the Fram Strait, the main gateway for Atlantic inflow into the Arctic Ocean. Cell abundances of the bacterioplankton communities in surface waters varied from 105 cells mL–1 in ice-covered regions to 106 cells mL–1 in the ice-free regions. Observations suggest that these were overall driven by variations in phytoplankton bloom conditions across the Strait. The bacterial groups Bacteroidetes and Gammaproteobacteria showed several-fold higher cell abundances under late phytoplankton bloom conditions of the ice-free regions. Other taxonomic groups, such as the Rhodobacteraceae, revealed a distinct association of cell abundances with the surface Atlantic waters. With increasing depth (>500 m), the total cell abundances of the bacterioplankton communities decreased by up to two orders of magnitude, while largely unknown taxonomic groups (e.g., SAR324 and SAR202 clades) maintained constant cell abundances throughout the entire water column (ca. 103 cells mL–1). This suggests that these enigmatic groups may occupy a specific ecological niche in the entire water column. Our results provide the first quantitative spatial variations assessment of bacterioplankton in the summer ice-covered and ice-free Arctic water column, and suggest that further shift toward ice-free Arctic summers with longer phytoplankton blooms can lead to major changes in the associated standing stock of the bacterioplankton communities.

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Pangenomics reveal diversification of enzyme families and niche specialization in globally abundant SAR202 bacteria

Abstract: 31 65 showing that metabolically diverse variants of these cells occupy niches spanning all 66 depths, and are not relegated to the dark ocean. 67

Cited by 4 publications

References 65 publications

Bulk and Active Sediment Prokaryotic Communities in the Mariana and Mussau Trenches

Bulk and Active Sediment Prokaryotic Communities in the Mariana and Mussau Trenches

Migratory Zooplankton Excreta and Its Influence on Prokaryotic Communities

Spatial Distribution of Arctic Bacterioplankton Abundance Is Linked to Distinct Water Masses and Summertime Phytoplankton Bloom Dynamics (Fram Strait, 79°N)

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