Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor

• Published in: mBio
• Main Authors: Vuillemin, Aurèle, Vargas, Sergio, Coskun, Ömer K., Pockalny, Robert, Murray, Richard W., Smith, David C, D'Hondt, Steven, Orsi, William D.
• Format: Text
• Language: unknown
• Published: DigitalCommons@URI 2020
• Subjects: North Atlantic
• Online Access: https://digitalcommons.uri.edu/gsofacpubs/734; https://doi.org/10.1128/mBio.01937-20; https://digitalcommons.uri.edu/context/gsofacpubs/article/1701/viewcontent/mBio_2020_Vuillemin_e01937_20.full.pdf

How microbial metabolism is translated into cellular reproduction under energy-limited settings below the seafloor over long timescales is poorly under- stood. 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 an- cient 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 con- sistent 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 sub- seafloor reproducing “Ca. Atribacteria” also expressed genes encoding a bacterial mi- crocompartment 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 func- tion. 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.