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    Publication Date: 2022-10-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Vuillemin, A., Vargas, S., Coskun, O. K., Pockalny, R., Murray, R. W., Smith, D. C., D'Hondt, S., & Orsi, W. D. Atribacteria reproducing over millions of years in the Atlantic abyssal subseafloor. Mbio, 11(5), (2020): e01937-20, doi:10.1128/mBio.01937-20.
    Description: 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.
    Description: This work was supported primarily by the Deutsche Forschungsgemeinschaft (DFG) project OR 417/1-1 granted to W.D.O. Preliminary work was supported by the Center for Dark Energy Biosphere Investigations project OCE-0939564 also granted to W.D.O. The expedition was funded by the US National Science Foundation through grant NSF-OCE-1433150 to S.D. and R.P. R.W.M. led the expedition. Shipboard microbiology efforts were supported by the Center for Dark Energy Biosphere Investigations (C-DEBI grant NSF-OCE-0939564). This is C-DEBI publication 545. This is a contribution of the Deep Carbon Observatory (DCO).
    Keywords: Deep biosphere ; Energy limit to life ; Atribacteria ; Acetogenesis ; Metagenomics ; Transcriptomics ; Fermentation ; Bacterial microcompartment ; Clade JS1 ; Metatranscriptomics ; Subseafloor life
    Repository Name: Woods Hole Open Access Server
    Type: Article
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