The majority of microorganisms in gas hydrate-bearing subseafloor sediments ferment macromolecules

Abstract

Background: Gas hydrate-bearing subseafloor sediments harbor a large number of microorganisms. Sedimentary organic matter and upward methane fluids represent two important sources of carbon and energy for deep biosphere. However, which metabolism dominates the deep subseafloor of gas hydrate zone is poorly constrained. Here we studied the microbial communities in gas-hydrate rich sediments up to 49 meters below seafloor recovered by drilling in the South China Sea. We focused on distinct geochemical conditions, and performed metagenomic and metatranscriptomic analyses to characterize microbial diversity and their role in carbon mineralization. Results: Comparative microbial community analysis revealed that samples above and in sulfate-methane interface (SMI) zones clearly distinguish from those below the SMI. Chloroflexota, are most abundant above the SMI, whereas Caldatribacteriota dominate below the SMI. Verrucomicrobiota, Bathyarchaeia and Hadarchaeota were similarly present in both types of sediment. The genomic inventory and transcriptional activity suggest roles in fermentation of macromolecule. By contrast, sulfate reducers and methanogens, organisms that catalyze the consumption or production of commonly observed chemical compounds in sediments are rare. Methanotrophs of the ANME-1 group thrived in or slightly below the current sulfate methane interface. Rare members from Heimdallarchaeia were identified to encode the potential for anaerobic oxidation of short-chain hydrocarbons. Conclusions: These findings indicate that fermentation of macromolecules is the predominant energy source for microorganisms in deep subseafloor sediments that are experiencing upward methane fluxes.

What is the role of microbes in gas hydrate formation and stability?

“…In deep subsurface hydrate sediments, Atribacterota (JS-1) and Chloroflexota dominate bacterial 16S rRNA gene sequences and Asgardarchaeota (formerly MBGB/DSAG) dominate archaeal 16S rRNA gene sequences; these trends have been observed for deep subsurface hydrate-bearing sediments around the Pacific Rim, including Nankai Trough (Katayama et al, 2016;Wellsbury et al, 2000), Umitaka Spur (Yanagawa et al, 2014), Ulleung Basin (Lee et al, 2013), Cascadia Margin (Parkes et al, 2014), Hydrate Ridge (Glass et al, 2021;Inagaki et al, 2006;Nunoura et al, 2008), and the Peru Margin (Inagaki et al, 2006). 16S rRNA gene sequences from the South China Sea differed between studies (Cui et al, 2019(Cui et al, , 2020Gong et al, 2017;Jiang et al, 2007;Jiao et al, 2015), but metagenomic sequencing shows dominance of Atribacterota (JS-1), Chloroflexota, and Asgardarchaeota (Zhang et al, 2022), consistent with other Pacific Rim sites. In contrast, 16S rRNA gene sequences from hydrate sediments from the Andaman Sea were dominated by Firmicutes, as were sediment isolates (Briggs et al, 2012;Parkes et al, 2009).…”

“…Hydrate sediments are extreme habitats with multiple stresses on microbial populations, including low temperatures, high pressures, high salt, low water activity, and, at greater sediment depths, limited pore space (Park & Santamarina, 2020; Phadnis & Santamarina, 2011). Microbial metabolisms and stress adaptions in hydrate sediments have been assessed with metagenomics, metagenome‐assembled genomes, and metatranscriptomics, revealing that most microbes that reside in hydrate‐bearing sediments are heterotrophs that ferment macromolecules (Dong et al, 2019; Zhang et al, 2022). However, a respiratory complex predicted to couple proton and sodium translocation to molecular hydrogen production using an evolutionarily distinct hydrogenase has been found in JS‐1 class of Atribacterota and several Firmicutes under Hydrate Ridge (Glass et al, 2021).…”

Unexpected genetic and microbial diversity for arsenic cycling in deep sea cold seep sediments

“…The 87 metagenomes and 33 metatranscriptomes analyzed in this study are derived from 13 globally distributed cold seep sites ( Supplementary Figure 1 ). Among them, 65 metagenomes and 10 metatranscriptomes were compiled from our previous publications 8, 59 , and other 22 metagenomes were downloaded from NCBI Sequencing Read Archive (SRA). A detailed description of sampling locations and sequencing information for metagenomic and metatranscriptomic data is given in Supplementary Data 1 .…”

A comprehensive catalog with 100 million genes and 3,000 metagenome-assembled genomes from global cold seep sediments

“…These sites are as follows: Eastern North Pacific (ENP), Santa Monica Mounds Bioinformatics Institute-European Nucleotide Archive (EBI-ENA) according to the accession numbers published in each study [8][9][10]35,[38][39][40][41] . The remaining 106 metagenomic datasets used in this study were obtained from our previous publications 7,12,[42][43][44][45][46][47][48][49] .…”