Functional diversity of microbial communities in inactive seafloor sulfide deposits

Abstract

The seafloor sulfide structures of inactive vents are known to host abundant and diverse microorganisms potentially supported by mineralogy of sulfides. However, little is known about the diversity and distribution of microbial functions. Here, we used genome-resolved metagenomics to predict microbial metabolic functions and the contribution of horizontal gene transfer to the functionality of microorganisms inhabiting several hydrothermally inactive seafloor deposits among globally distributed deep-sea vent fields. Despite of geographically distant vent fields, similar microbial community patterns were observed with the dominance of Gammaproteobacteria, Bacteroidota and previously overlooked Candidatus Patescibacteria. Metabolically flexible Gammaproteobacteria are major potential primary producers utilizing mainly sulfur, iron and hydrogen as electron donors coupled with oxygen and nitrate respiration for chemolithoautotrophic growth. In addition to heterotrophic microorganisms like free-living Bacteroidota, Ca. Patescibacteria potentially perform fermentative recycling of organic carbon. Finally, we provided evidence that many functional genes that are central to energy metabolism have been laterally transferred among members within the community and largely within the same class. Taken together, these findings shed light on microbial ecology and evolution in inactive seafloor sulfide deposits after the cessation of hydrothermal activities.

Metagenomics Reveals Dominant Unusual Sulfur Oxidizers Inhabiting Active Hydrothermal Chimneys From the Southwest Indian Ridge

“…Using these chimney samples, we report the genomes of dominant microbial species and the prevalence of distinct SOB affiliated with Campylobacterota, Gammaproteobacteria, and Alphaproteobacteria inhabiting the sulfide chimney, all of which have been reported in deep-sea cold seeps recently ( Li et al, 2021 ). The microbial community in the active SWIR hydrothermal vents was remarkably different from those from the SWIR inactive hydrothermal sulfide sediments ( Cao et al, 2014 ; Dong et al, 2021 ) and others DSHVs ( Dick, 2019 ; Hou et al, 2020 ; Zeng et al, 2021 ). Culturable Thiohalomonadales SOB, such as Thiohalomonas denitrificans had been isolated from the hydrothermal vents of the Suiyo Seamount in the Pacific Ocean ( Mori et al, 2015 ).…”

“…Prokaryotic communities in our chimney samples were examined by sequencing and analysis of 16S rRNA gene amplicons and 16S rRNA gene tags in metagenomic reads (16S miTags), and were then compared with those of the sulfide samples from other SWIR sites ( Supplementary Table 1 ; Dong et al, 2021 ). There are a total of 30,189 qualified 16S rRNA gene amplicons for the characterization of microbial communities.…”

“…In the periplasmic space, FccAB catalyzes oxidation of sulfide to elemental sulfur with electrons being transferred to cytochrome c; the SQR enzyme oxidizes sulfide to polysulfide ( Schutz et al, 1999 ). The DsrAB encoded by the SOB carry out sulfide oxidation to sulfite ( Anantharaman et al, 2014 ; Dong et al, 2021 ). This indicates the capacity of sulfide oxidation to S 0 , polysulfide or sulfate by these SOB bacteria inhabiting our active chimney samples under different fluxes of electron acceptors.…”

“…Thiomicrorhabdus has been reported as a dominant SOB in SWIR ( Cao et al, 2014 ), and was also isolated from the other hydrothermal vents ( Brazelton and Baross, 2010 ; Scott et al, 2019 ). A recent study revealed a large number of Gammaproteobacteria with sulfur oxidation potentials using nitrate and oxygen as electron acceptors in the SWIR inactive hydrothermal sediments ( Dong et al, 2021 ). We employed metagenomics to compare the microbiomes in the active hydrothermal vents with those from inactive ones to reveal microbial community structure and ecological function driven by active “black-smoker” hydrothermal seepage in SWIR.…”

“…Sulfur oxidizing bacteria (SOB) dominate various hydrothermal sediments and flumes and are classified to be aerobes (e.g., SUP05 and Beggiatoa from Gammaproteobacteria), microaerobes (e.g., Sulfurimonas and Sulfurovum from Epsilonbacteraeota), and anaerobes (e.g., Caminibacter and Nautila from Epsilonbacteraeota) ( López-García et al, 2003 ; Dick, 2019 ; Meier et al, 2019 ; Hou et al, 2020 ) with preference to different electron donors. For the microaerobic SOB, the cbb3 -type cytochrome c oxidase was involved in adaptation to low oxygen concentrations for respiration ( Hou et al, 2020 ; Dong et al, 2021 ); however, the mechanism for reducing the damage by high oxygen flux is largely unknown. Considering the highly variable microenvironments adjacent to an active hydrothermal vent, there are perhaps much more SOB species that have evolved to adapt to the varying temperature and redox conditions.…”