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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American Society for Microbiology
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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 |
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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 |
container_title |
mBio |
container_volume |
11 |
container_issue |
5 |
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1766134701628588032 |