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 five 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 a fermentative, and potentially acetogenic metabolism. “Ca. Atribacteria” dominated throughout the entire eight million-year-old cored sequence, despite the detection limit for gene expression being reached in five million-year-old sediments. The subseafloor reproducing “Ca. Atribacteria” also expressed genes encoding a bacterial micro-compartment 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.ImportanceThe 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 micro-compartment 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.

Quantifying the effects of hydrogen on carbon assimilation in a seafloor microbial community associated with ultramafic rocks

“…However, when H 2 is not present the activity of acetate kinase may be reversed and acetate is assimilated [64]. In line with our finding, it has been recently discussed that Atribacteria could use WLP either in catabolic or anabolic directions in deep subseafloor sediments [65].…”

Vertical diversity and association pattern of total, abundant and rare microbial communities in deep‐sea sediments

“…Concentrations of started to decrease below 190 cm, due to increased sulphate‐reducing bacteria including Desulfuromonadales, Desulfovibrionales, Desulfobacterales and Desulfarculales in Deltaproteobacteria. However, these sulphate‐reducing bacteria only accounted for a small proportion in Deltaproteobacteria, outcompeted by fermentative members of Chloroflexi (Dehalococcoides), Atribacteria and Aerophobetes (Kerrigan et al, 2020; Vuillemin, Vargas, et al, 2020; Wang & Li, 2016). Fermentation of organic acid was also achieved by several archaeal groups enriched in deep sediments, including Lokiarchaeota (Orsi et al, 2020) and Bathyarchaeota (He et al, 2016).…”

“…In‐depth knowledge of microbial biodiversity and interaction patterns is important for understanding these biogeographical processes, which is particularly true for the large and complex microbial populations in marine sediments (Hoshino et al, 2020). Previous studies have discussed vertical benthic microbial diversity in varied depth ranges (Inagaki et al, 2003, 2015; Nunoura et al, 2016, 2018; Schauer et al, 2010; Starnawski et al, 2017; Vuillemin, Vargas, et al, 2020; Vuillemin et al, 2019; Walsh et al, 2016), and highly resolved vertical profiles of microbial communities in sediments will help to better depict the stratified community structure and continuous variations in microbial diversity. However, so far, the majority of these studies have often focused on specific types of sedimentary environment (Nunoura et al, 2018; Yang et al, 2020) or comparison of microbial community over large spatial or temporal scales (Böer et al, 2009; Hoshino et al, 2020; Hoshino & Inagaki, 2019).…”

Microbial metabolism and adaptations in Atribacteria-dominated methane hydrate sediments

“…Marine Atribacteria are dispersed through ejection from submarine mud volcanoes (Hoshino et al, 2017; Ruff et al, 2019), and environmental heterogeneity may select for locally adapted genotypes. Atribacteria are highly enriched in anoxic, organic, and hydrocarbon rich sediments (Chakraborty et al, 2020; Hoshino et al, 2020) and have recently been discovered to be actively reproducing in the deep subsurface (Vuillemin et al, 2020). The phylogenetic diversity of Atribacteria genera suggests the potential for uncharacterized variation in functional niches.…”