D:L-Amino Acid Modeling Reveals Fast Microbial Turnover of Days to Months in the Subsurface Hydrothermal Sediment of Guaymas Basin

Møller, Mikkel H.; Glombitza, Clemens; Lever, Mark A.; Deng, Longhui; Morono, Yuki; Inagaki, Fumio; Doll, Mechthild; Su, Chih-Chiang; Lomstein, Bente Aa.

doi:10.3389/fmicb.2018.00967

Cited by 25 publications

(20 citation statements)

References 52 publications

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“…Atribacteria," indicating the exponential growth phase (43). Thus, while we do not report measurements of biomass turnover such as amino acid racemization (44,45) or stable isotope probing (4,17), the steadily increasing microbial biomass of "Ca. Atribacteria" with increasing sediment depth together with the detected correlation between their abundance and transcriptional activity ( Fig.…”

Section: Resultsmentioning

confidence: 86%

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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Section: Resultsmentioning

confidence: 86%

Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor

Vuillemin

Vargas

Coskun

et al. 2020

mBio

View full text Add to dashboard Cite

show abstract

“…Atribacteria", indicating exponential growth phase (43). Thus, while we do not report measurements of biomass turnover such as amino acid racemization (44,45) or stable isotope probing (4,17), the steadily increasing microbial biomass of "Ca. Atribacteria" with increasing sediment depth together with the detected correlation between their abundance and transcriptional activity (Fig.…”

Section: Gene Expression Analysismentioning

confidence: 84%

Atribacteria reproducing over millions of years in the Atlantic abyssal subseafloor

Vuillemin

Vargas

Coskun

et al. 2020

Preprint

View full text Add to dashboard Cite

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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“…These variables affect the power requirements of microbial life, e.g., by increasing rates of biomolecule damage, and consequently also raise the power required by cells to maintain and repair essential biomolecules (Lever et al, 2015). As a result, the presence and abundance of microorganisms within subseafloor habitats varies greatly with location as a result of stark differences in cell-specific power supply and cell-specific power demand (Inagaki et al, 2015; Lever et al, 2015; Møller et al, 2018; Heuer et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Origin of Short-Chain Organic Acids in Serpentinite Mud Volcanoes of the Mariana Convergent Margin

et al. 2019

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Serpentinitic systems are potential habitats for microbial life due to frequently high concentrations of microbial energy substrates, such as hydrogen (H 2 ), methane (CH 4 ), and short-chain organic acids (SCOAs). Yet, many serpentinitic systems are also physiologically challenging environments due to highly alkaline conditions (pH > 10) and elevated temperatures (>80°C). To elucidate the possibility of microbial life in deep serpentinitic crustal environments, International Ocean Discovery Program (IODP) Expedition 366 drilled into the Yinazao, Fantangisña, and Asùt Tesoru serpentinite mud volcanoes on the Mariana Forearc. These mud volcanoes differ in temperature (80, 150, 250°C, respectively) of the underlying subducting slab, and in the porewater pH (11.0, 11.2, 12.5, respectively) of the serpentinite mud. Increases in formate and acetate concentrations across the three mud volcanoes, which are positively correlated with temperature in the subducting slab and coincide with strong increases in H 2 concentrations, indicate a serpentinization-related origin. Thermodynamic calculations suggest that formate is produced by equilibrium reactions with dissolved inorganic carbon (DIC) + H 2 , and that equilibration continues during fluid ascent at temperatures below 80°C. By contrast, the mechanism(s) of acetate production are not clear. Besides formate, acetate, and H 2 data, we present concentrations of other SCOAs, methane, carbon monoxide, and sulfate, δ 13 C-data on bulk carbon pools, and microbial cell counts. Even though calculations indicate a wide range of microbial catabolic reactions to be thermodynamically favorable, concentration profiles of potential energy substrates, and very low cell numbers suggest that microbial life is scarce or absent. We discuss the potential roles of temperature, pH, pressure, and dispersal in limiting the occurrence of microbial life in deep serpentinitic environments.

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D:L-Amino Acid Modeling Reveals Fast Microbial Turnover of Days to Months in the Subsurface Hydrothermal Sediment of Guaymas Basin

Cited by 25 publications

References 52 publications

Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor

Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor

Atribacteria reproducing over millions of years in the Atlantic abyssal subseafloor

Origin of Short-Chain Organic Acids in Serpentinite Mud Volcanoes of the Mariana Convergent Margin

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