Homoacetogenesis in Deep-Sea
            <i>Chloroflexi</i>
            , as Inferred by Single-Cell Genomics, Provides a Link to Reductive Dehalogenation in Terrestrial
            <i>Dehalococcoidetes</i>

Sewell, Holly L.; Kaster, Anne‐Kristin; Spormann, Alfred M.

doi:10.1128/mbio.02022-17

Cited by 32 publications

(22 citation statements)

References 111 publications

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“…6), including those affiliated with phyla previously inferred to mediate acetogenesis in deep-sea sediments through either the tetrahydrofolate-dependent bacterial pathway (e.g. Chloroflexi and Aerophobetes) 5,28 or the tetrahydromethanopterin-dependent archaeal variant (e.g. Bathyarchaeota and Asgard group) 29,30 .…”

Section: Resultsmentioning

confidence: 99%

Metabolic potential of uncultured bacteria and archaea associated with petroleum seepage in deep-sea sediments

et al. 2019

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The lack of microbial genomes and isolates from the deep seabed means that very little is known about the ecology of this vast habitat. Here, we investigate energy and carbon acquisition strategies of microbial communities from three deep seabed petroleum seeps (3 km water depth) in the Eastern Gulf of Mexico. Shotgun metagenomic analysis reveals that each sediment harbors diverse communities of chemoheterotrophs and chemolithotrophs. We recovered 82 metagenome-assembled genomes affiliated with 21 different archaeal and bacterial phyla. Multiple genomes encode enzymes for anaerobic oxidation of aliphatic and aromatic compounds, including those of candidate phyla Aerophobetes, Aminicenantes, TA06 and Bathyarchaeota. Microbial interactions are predicted to be driven by acetate and molecular hydrogen. These findings are supported by sediment geochemistry, metabolomics, and thermodynamic modelling. Overall, we infer that deep-sea sediments experiencing thermogenic hydrocarbon inputs harbor phylogenetically and functionally diverse communities potentially sustained through anaerobic hydrocarbon, acetate and hydrogen metabolism.

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Section: Resultsmentioning

confidence: 99%

Metabolic potential of uncultured bacteria and archaea associated with petroleum seepage in deep-sea sediments

et al. 2019

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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 ϩ and oxidized ferredoxin to thereby increase anaerobic metabolic efficiency (61).…”

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: 89%

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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Homoacetogenesis in Deep-Sea Chloroflexi , as Inferred by Single-Cell Genomics, Provides a Link to Reductive Dehalogenation in Terrestrial Dehalococcoidetes

Cited by 32 publications

References 111 publications

Metabolic potential of uncultured bacteria and archaea associated with petroleum seepage in deep-sea sediments

Metabolic potential of uncultured bacteria and archaea associated with petroleum seepage in deep-sea sediments

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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