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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Published in:mBio
Main Authors: Aurèle Vuillemin, Sergio Vargas, Ömer K. Coskun, Robert Pockalny, Richard W. Murray, David C. Smith, Steven D’Hondt, William D. Orsi
Format: Article in Journal/Newspaper
Language:English
Published: American Society for Microbiology 2020
Subjects:
Online Access:https://doi.org/10.1128/mBio.01937-20
https://doaj.org/article/caa413abe2bd4871bc3b8f2e3a78218d
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spelling ftdoajarticles:oai:doaj.org/article:caa413abe2bd4871bc3b8f2e3a78218d 2023-05-15T17:35:31+02:00 Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor Aurèle Vuillemin Sergio Vargas Ömer K. Coskun Robert Pockalny Richard W. Murray David C. Smith Steven D’Hondt William D. Orsi 2020-10-01T00:00:00Z https://doi.org/10.1128/mBio.01937-20 https://doaj.org/article/caa413abe2bd4871bc3b8f2e3a78218d EN eng American Society for Microbiology https://journals.asm.org/doi/10.1128/mBio.01937-20 https://doaj.org/toc/2150-7511 doi:10.1128/mBio.01937-20 2150-7511 https://doaj.org/article/caa413abe2bd4871bc3b8f2e3a78218d mBio, Vol 11, Iss 5 (2020) deep biosphere energy limit to life atribacteria acetogenesis metagenomics transcriptomics Microbiology QR1-502 article 2020 ftdoajarticles https://doi.org/10.1128/mBio.01937-20 2022-12-31T09:14:52Z 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 ... Article in Journal/Newspaper North Atlantic Directory of Open Access Journals: DOAJ Articles mBio 11 5
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
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
topic_facet deep biosphere
energy limit to life
atribacteria
acetogenesis
metagenomics
transcriptomics
Microbiology
QR1-502
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 ...
format Article in Journal/Newspaper
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://doi.org/10.1128/mBio.01937-20
https://doaj.org/article/caa413abe2bd4871bc3b8f2e3a78218d
genre North Atlantic
genre_facet North Atlantic
op_source mBio, Vol 11, Iss 5 (2020)
op_relation https://journals.asm.org/doi/10.1128/mBio.01937-20
https://doaj.org/toc/2150-7511
doi:10.1128/mBio.01937-20
2150-7511
https://doaj.org/article/caa413abe2bd4871bc3b8f2e3a78218d
op_doi https://doi.org/10.1128/mBio.01937-20
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