Cellular content of biomolecules in sub-seafloor microbial communities

Braun, S.; Morono, Yuki; Becker, Kevin W.; Hinrichs, Kai‐Uwe; Kjeldsen, Kasper Urup; Jørgensen, Bo Barker; Lomstein, Bente Aa.

doi:10.1016/j.gca.2016.06.019

Cited by 19 publications

(25 citation statements)

References 77 publications

(102 reference statements)

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“…Although these phylogenetically and physiologically diverse bacteria exhibit a similar trend toward phosphorus-lacking lipids, the synthesis of MGDG as the major glycolipid appears to be a distinct feature of phosphorus-limited G20. Similar prevalence of MGDG was previously reported in environmental samples [20, 21], but not in culture experiments.…”

Section: Discussionsupporting

confidence: 90%

System-Wide Adaptations of Desulfovibrio alaskensis G20 to Phosphate-Limited Conditions

et al. 2016

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The prevalence of lipids devoid of phosphorus suggests that the availability of phosphorus limits microbial growth and activity in many anoxic, stratified environments. To better understand the response of anaerobic bacteria to phosphate limitation and starvation, this study combines microscopic and lipid analyses with the measurements of fitness of pooled barcoded transposon mutants of the model sulfate reducing bacterium Desulfovibrio alaskensis G20. Phosphate-limited G20 has lower growth rates and replaces more than 90% of its membrane phospholipids by a mixture of monoglycosyl diacylglycerol (MGDG), glycuronic acid diacylglycerol (GADG) and ornithine lipids, lacks polyphosphate granules, and synthesizes other cellular inclusions. Analyses of pooled and individual mutants reveal the importance of the high-affinity phosphate transport system (the Pst system), PhoR, and glycolipid and ornithine lipid synthases during phosphate limitation. The phosphate-dependent synthesis of MGDG in G20 and the widespread occurrence of the MGDG/GADG synthase among sulfate reducing ∂-Proteobacteria implicate these microbes in the production of abundant MGDG in anaerobic environments where the concentrations of phosphate are lower than 10 μM. Numerous predicted changes in the composition of the cell envelope and systems involved in transport, maintenance of cytoplasmic redox potential, central metabolism and regulatory pathways also suggest an impact of phosphate limitation on the susceptibility of sulfate reducing bacteria to other anthropogenic or environmental stresses.

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Section: Discussionsupporting

confidence: 90%

System-Wide Adaptations of Desulfovibrio alaskensis G20 to Phosphate-Limited Conditions

et al. 2016

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“…Differences in the number of reads mapped on SAGs do explain some of the diversity differences observed, but genuine differences among lineages remain (P = 0.016). Our generation time estimate is based on empirically determined parameters (Material and Methods); of these, cellular carbon content varies twofold (27) and sediment age by 2% (4), whereas rates of carbon mineralization were modeled from experimental data with a SD of 5% (19,28). Finally, cellular growth yields likely vary by a factor of 2-3, according to pure culture studies and subsurface sediment modeling (3,6,8).…”

Section: Resultsmentioning

confidence: 99%

“…We therefore used such a power law function determined for Aarhus Bay sediments (19) to calculate organic carbon oxidation rates. Cell-specific carbon oxidation rates were calculated from total cell abundances and were used to estimate biomass turnover of cells assuming a growth yield of 8% (8) and a cellular carbon content of 21.5 fg (27). The biomass turnover serves as a proxy for the generation times of cells assuming that the cells indeed are growing by cell division in the energydepleted subseafloor as opposed to being in a nongrowth state where cells merely repair and sustain their biomolecules (9).…”

Section: Methodsmentioning

confidence: 99%

Microbial community assembly and evolution in subseafloor sediment

Starnawski

Bataillon

Ettema

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Bacterial and archaeal communities inhabiting the subsurface seabed live under strong energy limitation and have growth rates that are orders of magnitude slower than laboratory-grown cultures. It is not understood how subsurface microbial communities are assembled and whether populations undergo adaptive evolution or accumulate mutations as a result of impaired DNA repair under such energy-limited conditions. Here we use amplicon sequencing to explore changes of microbial communities during burial and isolation from the surface to the >5,000-y-old subsurface of marine sediment and identify a small core set of mostly uncultured bacteria and archaea that is present throughout the sediment column. These persisting populations constitute a small fraction of the entire community at the surface but become predominant in the subsurface. We followed patterns of genome diversity with depth in four dominant lineages of the persisting populations by mapping metagenomic sequence reads onto single-cell genomes. Nucleotide sequence diversity was uniformly low and did not change with age and depth of the sediment. Likewise, there was no detectable change in mutation rates and efficacy of selection. Our results indicate that subsurface microbial communities predominantly assemble by selective survival of taxa able to persist under extreme energy limitation.acteria and archaea inhabiting the subsurface seabed account for more than half of all microbial cells in the oceans (1, 2). The subsurface communities are cut off from fresh detrital organic matter deposited on the sea floor. The energy available for cellular maintenance and growth decreases rapidly with depth and age of the sediment (3-5). As a consequence, the microbial abundance and cell-specific metabolic rates decrease by orders of magnitude already within the top few meters of sediment (3, 6-8). However, even hundreds of meters below the seafloor sediments are populated by microbes that actively turn over their biomass (3,8). The growth characteristics of these microbial populations are unlike anything studied in pure culture as estimates suggest that the generation times of subsurface cells are tens to hundreds of years (3,7,8). As a model for how these deep biosphere communities are assembled, it was suggested that the microbes found in the subsurface seabed represent descendants of surface communities that were buried in the past (9-12). So far this model has not been tested systematically. Furthermore, it is not known if subsurface microorganisms during the burial evolve unique genetic traits conferring adaptation to this environment (13). Studies of adaptation and evolution in freeliving microorganisms reported high genetic heterogeneity and rapid evolutionary change within natural populations. However, these studies have focused on dynamic or mixed environments with large population sizes and rapid growth, e.g., biofilms or planktonic communities (14-16) that are very different from the subsurface seabed environment.According to "Drake's rule" (17), DNA-based or...

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“…Cell extracts from density centrifugation were then subjected to extensive cell purification using FACS to remove detrital particles as described in Braun et al (2016). …”

Section: Methodsmentioning

confidence: 99%

Size and Carbon Content of Sub-seafloor Microbial Cells at Landsort Deep, Baltic Sea

et al. 2016

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The discovery of a microbial ecosystem in ocean sediments has evoked interest in life under extreme energy limitation and its role in global element cycling. However, fundamental parameters such as the size and the amount of biomass of sub-seafloor microbial cells are poorly constrained. Here we determined the volume and the carbon content of microbial cells from a marine sediment drill core retrieved by the Integrated Ocean Drilling Program (IODP), Expedition 347, at Landsort Deep, Baltic Sea. To determine their shape and volume, cells were separated from the sediment matrix by multi-layer density centrifugation and visualized via epifluorescence microscopy (FM) and scanning electron microscopy (SEM). Total cell-carbon was calculated from amino acid-carbon, which was analyzed by high-performance liquid chromatography (HPLC) after cells had been purified by fluorescence-activated cell sorting (FACS). The majority of microbial cells in the sediment have coccoid or slightly elongated morphology. From the sediment surface to the deepest investigated sample (~60 m below the seafloor), the cell volume of both coccoid and elongated cells decreased by an order of magnitude from ~0.05 to 0.005 μm3. The cell-specific carbon content was 19–31 fg C cell−1, which is at the lower end of previous estimates that were used for global estimates of microbial biomass. The cell-specific carbon density increased with sediment depth from about 200 to 1000 fg C μm−3, suggesting that cells decrease their water content and grow small cell sizes as adaptation to the long-term subsistence at very low energy availability in the deep biosphere. We present for the first time depth-related data on the cell volume and carbon content of sedimentary microbial cells buried down to 60 m below the seafloor. Our data enable estimates of volume- and biomass-specific cellular rates of energy metabolism in the deep biosphere and will improve global estimates of microbial biomass.

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Cellular content of biomolecules in sub-seafloor microbial communities

Cited by 19 publications

References 77 publications

System-Wide Adaptations of Desulfovibrio alaskensis G20 to Phosphate-Limited Conditions

System-Wide Adaptations of Desulfovibrio alaskensis G20 to Phosphate-Limited Conditions

Microbial community assembly and evolution in subseafloor sediment

Size and Carbon Content of Sub-seafloor Microbial Cells at Landsort Deep, Baltic Sea

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