Metagenomic Features Characterized with Microbial Iron Oxidoreduction and Mineral Interaction in Southwest Indian Ridge

The Southwest Indian Ridge (SWIR) is one of the typical representatives of deep-sea ultraslow-spreading ridges, and has increasingly become a hot spot of studying subsurface geological activities and deep-sea mining management. However, the understanding of microbial activities is still limited on active hydrothermal vent chimneys in SWIR. In this study, samples from an active black smoker and a diffuse vent located in the Longqi hydrothermal region were collected for deep metagenomic sequencing, which yielded approximately 290 GB clean data and 295 mid-to-high-quality metagenome-assembled genomes (MAGs). Sulfur oxidation conducted by a variety of Gammaproteobacteria, Alphaproteobacteria, and Campylobacterota was presumed to be the major energy source for chemosynthesis in Longqi hydrothermal vents. Diverse iron-related microorganisms were recovered, including iron-oxidizing Zetaproteobacteria, iron-reducing Deferrisoma, and magnetotactic bacterium. Twenty-two bacterial MAGs from 12 uncultured phyla harbored iron oxidase Cyc2 homologs and enzymes for organic carbon degradation, indicated novel chemolithoheterotrophic iron-oxidizing bacteria that affected iron biogeochemistry in hydrothermal vents. Meanwhile, potential interactions between microbial communities and chimney minerals were emphasized as enriched metabolic potential of siderophore transportation, and extracellular electron transfer functioned by multi-heme proteins was discovered. Composition of chimney minerals probably affected microbial iron metabolic potential, as pyrrhotite might provide more available iron for microbial communities. Collectively, this study provides novel insights into microbial activities and potential mineral-microorganism interactions in hydrothermal vents. IMPORTANCE Microbial activities and interactions with minerals and venting fluid in active hydrothermal vents remain unclear in the ultraslow-spreading SWIR (Southwest Indian Ridge). Understanding about how minerals influence microbial metabolism is currently limited given the obstacles in cultivating microorganisms with sulfur or iron oxidoreduction functions. Here, comprehensive descriptions on microbial composition and metabolic profile on 2 hydrothermal vents in SWIR were obtained based on cultivation-free metagenome sequencing. In particular, autotrophic sulfur oxidation supported by minerals was presumed, emphasizing the role of chimney minerals in supporting chemosynthesis. Presence of novel heterotrophic iron-oxidizing bacteria was also indicated, suggesting overlooked biogeochemical pathways directed by microorganisms that connected sulfide mineral dissolution and organic carbon degradation in hydrothermal vents. Our findings offer novel insights into microbial function and biotic interactions on minerals in ultraslow-spreading ridges.