Metagenomic insights into the metabolic versatility in iron-rich mats of the lucky strike hydrothermal field

Abstract

Iron-rich microbial mats from the Lucky Strike Hydrothermal Field represent critical interfaces between geochemical energy sources and carbon cycling. While the taxonomic diversity of these mats has been explored in previous studies, their functional diversity and metabolic potential remain less understood. It is the aim of this study with an emphasized focus on carbon fixation and iron oxidation, using metagenomic sequencing and metabolic pathways analysis of microbial communities from four distinct iron-rich microbial mats (CAP, NTE, LL, Y3). A total of 1,765 medium- to high-quality metagenome-assembled genomes were reconstructed, spanning 85 phyla and 739 families. Twenty-eight families were common across all sites, including two families of iron-oxidizing bacteria from Mariprofundales order. Site-specific families such as Methanocomedenaceae (Y3) and members of the phylum Planctomycetota (LL) were highlighted. Beta-diversity analysis revealed a differentiation by site, with a marked taxonomic resemblance at CAP and NTE while those of Y3 and particularly LL were distinctly separated. Distance-based redundancy analysis highlighted the pivotal role of iron availability and substratum type in shaping microbial communities across sites. Functional profiling analysis revealed distinct clustering by site, with variation primarily associated with autotrophic pathways, methanotrophy and anaerobic respiration. Prediction of potential metabolic pathways showed that inorganic carbon fixation pathways varied significantly among sites. Methanotrophy, mediated mainly by Methanocomedenaceae and Methylomonadaceae families, tended to be highest at Y3. Among metal oxidation pathways, iron oxidation emerged as the prevalent energy source across all sites. At the class level, contributions of Gammaproteobacteria and Alphaproteobacteria were dominant, except at Y3, where contribution of Zetaproteobacteria was comparable. At the family level, Mariprofundaceae was identified as a ubiquitous contributor across all sites. Sixty-five Zetaproteobacteria MAGs were reconstructed, most harboring the cyc2 gene from cluster 1. Additionally, three Ghiorsea MAGs contained the grc gene cluster. This study highlights the functional specialization of LSHF iron-rich microbial mats, driven by site-specific hydrothermal and mineralogical conditions. The distinct potential metabolic pathways and taxonomic diversity observed across sites reflect the influence of local environmental factors The coexistence of autotrophic, methanotrophic, and heterotrophic metabolisms underscores the ecological versatility of these communities and their significant contributions to carbon and iron cycling in these deep-sea iron-rich ecosystems.