Metabolic strategies of marine subseafloor Chloroflexi inferred from genome reconstructions

Fincker, Maeva; Huber, J. A.; Orphan, Victoria J.; Rappé, Michael S.; Teske, Andreas; Spormann, Alfred M.

doi:10.1111/1462-2920.15061

Cited by 61 publications

(66 citation statements)

References 102 publications

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“…Although Dehalococcoidia are generally considered as strictly anaerobic bacteria, they also appear in aerobic Community 10. The Anaerolineae includes isolates capable of aerobic growth (55), which is in good agreement with the potential for catabolic O 2 reduction inferred for related taxa from metagenomes (56)(57)(58). The members of Proteobacteria in Community 1 include taxa assigned to families with members involved in metal cycling in manganese nodules and manganese crusts, such as Magnetospiraceae (microaerobic heterotrophs) and Kiloniellaceae (59) (reported to be chemoheterotrophic aerobes; refs.…”

Section: Oxicsupporting

confidence: 69%

Global diversity of microbial communities in marine sediment

Hoshino

Doi

Uramoto

et al. 2020

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

248

150

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Microbial life in marine sediment contributes substantially to global biomass and is a crucial component of the Earth system. Subseafloor sediment includes both aerobic and anaerobic microbial ecosystems, which persist on very low fluxes of bioavailable energy over geologic time. However, the taxonomic diversity of the marine sedimentary microbial biome and the spatial distribution of that diversity have been poorly constrained on a global scale. We investigated 299 globally distributed sediment core samples from 40 different sites at depths of 0.1 to 678 m below the seafloor. We obtained ∼47 million 16S ribosomal RNA (rRNA) gene sequences using consistent clean subsampling and experimental procedures, which enabled accurate and unbiased comparison of all samples. Statistical analysis reveals significant correlations between taxonomic composition, sedimentary organic carbon concentration, and presence or absence of dissolved oxygen. Extrapolation with two fitted species–area relationship models indicates taxonomic richness in marine sediment to be 7.85 × 103 to 6.10 × 105 and 3.28 × 104 to 2.46 × 106 amplicon sequence variants for Archaea and Bacteria, respectively. This richness is comparable to the richness in topsoil and the richness in seawater, indicating that Bacteria are more diverse than Archaea in Earth’s global biosphere.

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Section: Oxicsupporting

confidence: 69%

Global diversity of microbial communities in marine sediment

Hoshino

Doi

Uramoto

et al. 2020

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

248

150

View full text Add to dashboard Cite

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“…The Wood-Ljungdahl pathway (WLP) has been found to be a widespread and potentially important metabolic pathway in subsurface microbial life ( 57 , 59 , 60 ). The WLP can be used catabolically to achieve redox balance and regenerate NAD + and oxidized ferredoxin to thereby increase anaerobic metabolic efficiency ( 61 ).…”

Section: Resultsmentioning

confidence: 99%

“…1A ) and relatively low rates of organic matter burial at our sampled site ( 11 , 19 ). In contrast, Chloroflexi related to Dehalococcoidia , which are predicted (homo)acetogens with metabolic potential to degrade complex organic compounds ( 59 , 60 ), are relatively abundant in these deep-sea anoxic clays ( Fig. 1B and C ) and transcribe genes involved in cell division ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor

Vuillemin

Vargas

Coskun

et al. 2020

mBio

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How microbial metabolism is translated into cellular reproduction under energy-limited settings below the seafloor over long timescales is poorly understood. Here, we show that microbial abundance increases an order of magnitude over a 5 million-year-long sequence in anoxic subseafloor clay of the abyssal North Atlantic Ocean. This increase in biomass correlated with an increased number of transcribed protein-encoding genes that included those involved in cytokinesis, demonstrating that active microbial reproduction outpaces cell death in these ancient sediments. Metagenomes, metatranscriptomes, and 16S rRNA gene sequencing all show that the actively reproducing community was dominated by the candidate phylum “Candidatus Atribacteria,” which exhibited patterns of gene expression consistent with fermentative, and potentially acetogenic, metabolism. “Ca. Atribacteria” dominated throughout the 8 million-year-old cored sequence, despite the detection limit for gene expression being reached in 5 million-year-old sediments. The subseafloor reproducing “Ca. Atribacteria” also expressed genes encoding a bacterial microcompartment that has potential to assist in secondary fermentation by recycling aldehydes and, thereby, harness additional power to reduce ferredoxin and NAD+. Expression of genes encoding the Rnf complex for generation of chemiosmotic ATP synthesis were also detected from the subseafloor “Ca. Atribacteria,” as well as the Wood-Ljungdahl pathway that could potentially have an anabolic or catabolic function. The correlation of this metabolism with cytokinesis gene expression and a net increase in biomass over the million-year-old sampled interval indicates that the “Ca. Atribacteria” can perform the necessary catabolic and anabolic functions necessary for cellular reproduction, even under energy limitation in millions-of-years-old anoxic sediments. IMPORTANCE The deep subseafloor sedimentary biosphere is one of the largest ecosystems on Earth, where microbes subsist under energy-limited conditions over long timescales. It remains poorly understood how mechanisms of microbial metabolism promote increased fitness in these settings. We discovered that the candidate bacterial phylum “Candidatus Atribacteria” dominated a deep-sea subseafloor ecosystem, where it exhibited increased transcription of genes associated with acetogenic fermentation and reproduction in million-year-old sediment. We attribute its improved fitness after burial in the seabed to its capabilities to derive energy from increasingly oxidized metabolites via a bacterial microcompartment and utilize a potentially reversible Wood-Ljungdahl pathway to help meet anabolic and catabolic requirements for growth. Our findings show that “Ca. Atribacteria” can perform all the necessary catabolic and anabolic functions necessary for cellular reproduction, even under energy limitation in anoxic sediments that are millions of years old.

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“…1A) and relatively low rates of organic matter burial at our sampled site (11,19). In contrast, Chloroflexi related to Dehalococcoidia, which are predicted (homo)acetogens with metabolic potential to degrade complex organic compounds (72,73), are relatively abundant in these deep-sea anoxic clay (Figs. 1B-C) and transcribe genes involved in cell division (Figs.…”

Section: Gene Expression Analysismentioning

confidence: 90%

Atribacteria reproducing over millions of years in the Atlantic abyssal subseafloor

Vuillemin

Vargas

Coskun

et al. 2020

Preprint

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How microbial metabolism is translated into cellular reproduction under energy-limited settings below the seafloor over long timescales is poorly understood. Here, we show that microbial abundance increases an order of magnitude over a five million-year-long sequence in anoxic subseafloor clay of the abyssal North Atlantic Ocean. This increase in biomass correlated with an increased number of transcribed protein-encoding genes that included those involved in cytokinesis, demonstrating that active microbial reproduction outpaces cell death in these ancient sediments. Metagenomes, metatranscriptomes, and 16S rRNA gene sequencing all show that the actively reproducing community was dominated by the candidate Phylum “Candidatus Atribacteria”, which exhibited patterns of gene expression consistent with a fermentative, and potentially acetogenic metabolism. “Ca. Atribacteria” dominated throughout the entire eight million-year-old cored sequence, despite the detection limit for gene expression being reached in five million-year-old sediments. The subseafloor reproducing “Ca. Atribacteria” also expressed genes encoding a bacterial micro-compartment that has potential to assist in secondary fermentation by recycling aldehydes and, thereby, harness additional power to reduce ferredoxin and NAD+. Expression of genes encoding the Rnf complex for generation of chemiosmotic ATP synthesis were also detected from the subseafloor “Ca. Atribacteria”, as well as the Wood-Ljungdahl pathway that could potentially have an anabolic or catabolic function. The correlation of this metabolism with cytokinesis gene expression and a net increase in biomass over the million-year-old sampled interval indicates that the “Ca. Atribacteria” can perform the necessary catabolic and anabolic functions necessary for cellular reproduction, even under energy limitation in millions of years old anoxic sediments.ImportanceThe deep subseafloor sedimentary biosphere is one of the largest ecosystems on Earth, where microbes subsist under energy-limited conditions over long timescales. It remains poorly understood how mechanisms of microbial metabolism promote increased fitness in these settings. We discovered that the candidate bacterial Phylum “Candidatus Atribacteria” dominated a deep-sea subseafloor ecosystem, where it exhibited increased transcription of genes associated with acetogenic fermentation and reproduction in million-year old sediment. We attribute its improved fitness after burial in the seabed to its capabilities to derive energy from increasingly oxidized metabolites via a bacterial micro-compartment and utilize a potentially reversible Wood-Ljungdahl pathway to help meet anabolic and catabolic requirements for growth. Our findings show that “Ca. Atribacteria” can perform all the necessary catabolic and anabolic functions necessary for cellular reproduction, even under energy limitation in anoxic sediments that are millions of years old.

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Metabolic strategies of marine subseafloor Chloroflexi inferred from genome reconstructions

Cited by 61 publications

References 102 publications

Global diversity of microbial communities in marine sediment

Global diversity of microbial communities in marine sediment

Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor

Atribacteria reproducing over millions of years in the Atlantic abyssal subseafloor

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