Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor

ABSTRACT 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...

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Autores principales:	Aurèle Vuillemin, Sergio Vargas, Ömer K. Coskun, Robert Pockalny, Richard W. Murray, David C. Smith, Steven D’Hondt, William D. Orsi
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	deep biosphere energy limit to life atribacteria acetogenesis metagenomics transcriptomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/caa413abe2bd4871bc3b8f2e3a78218d
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spelling	oai:doaj.org-article:caa413abe2bd4871bc3b8f2e3a78218d2021-11-15T16:19:09ZAtribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor10.1128/mBio.01937-202150-7511https://doaj.org/article/caa413abe2bd4871bc3b8f2e3a78218d2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01937-20https://doaj.org/toc/2150-7511ABSTRACT 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.Aurèle VuilleminSergio VargasÖmer K. CoskunRobert PockalnyRichard W. MurrayDavid C. SmithSteven D’HondtWilliam D. OrsiAmerican Society for Microbiologyarticledeep biosphereenergy limit to lifeatribacteriaacetogenesismetagenomicstranscriptomicsMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	deep biosphere energy limit to life atribacteria acetogenesis metagenomics transcriptomics Microbiology QR1-502
spellingShingle	deep biosphere energy limit to life atribacteria acetogenesis metagenomics transcriptomics Microbiology QR1-502 Aurèle Vuillemin Sergio Vargas Ömer K. Coskun Robert Pockalny Richard W. Murray David C. Smith Steven D’Hondt William D. Orsi Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor
description	ABSTRACT 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.
format	article
author	Aurèle Vuillemin Sergio Vargas Ömer K. Coskun Robert Pockalny Richard W. Murray David C. Smith Steven D’Hondt William D. Orsi
author_facet	Aurèle Vuillemin Sergio Vargas Ömer K. Coskun Robert Pockalny Richard W. Murray David C. Smith Steven D’Hondt William D. Orsi
author_sort	Aurèle Vuillemin
title	Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor
title_short	Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor
title_full	Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor
title_fullStr	Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor
title_full_unstemmed	Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor
title_sort	atribacteria reproducing over millions of years in the atlantic abyssal subseafloor
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/caa413abe2bd4871bc3b8f2e3a78218d
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Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor

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