Metabolic diversity of the Ferrovales and potential contributions to iron oxidation

Abstract Active and abandoned metal and coal mines generate acidic, metal-laden water that pollutes downstream areas, commonly referred to as acid mine drainage (AMD). AMD is host to microbial communities, including acidophilic iron oxidizers. Microbially-mediated iron oxidation is a desirable (bio)remediation strategy for AMD. Ferrovales are a common Fe-oxidizing bacterial group observed in AMD globally and thus could be an exceptional target for bioremediation strategies. However, Ferrovales are difficult to culture and both phylogenetically and metabolically diverse. To better understand the potential for Ferrovales to contribute to AMD bioremediation, we circumvented limitations in culture-based approaches and analyzed 240 genomes and metagenome assembled genomes from the Ferrovales, including taxa from AMD sites with high iron oxidation rates. The phylogenetic and physiological diversity of this group was greater than previously known and multiple Ferrovales taxa can co-occur. For example, we observed taxa that varied in mobility (based on the presence or absence of flagellar biosynthesis genes) and taxa that encode multiple iron oxidation pathways. We also identified Ferrovales that are likely capable of anoxygenic photosynthesis. Our data suggest that differences in physiology promote niche differentiation along resource axes and co-occurrence of multiple taxa. It’s possible that multiple co-occurring iron oxidizing taxa could support a more robust microbial community, resulting in higher iron oxidation rates and more efficient bioremediation. Importance Acid mine drainage (AMD) pollutes watersheds worldwide. Microbial communities can be leveraged to improve AMD bioremediation, the use of living things for the remediation of contaminated sites, because they drive biogeochemical processes in these ecosystems. Iron-oxidizing microbial species remove iron from AMD effluent, and the iron oxides sorb other trace metals. These communities vary across sites and differ in how rapidly they oxidize iron. Therefore, it is difficult to effectively use them for bioremediation. Ferrovales are common iron-oxidizing taxa in AMD globally, including in sites with exceptionally high rates of iron oxidation. To examine the potential for Ferrovales to be key components of bioremediation strategies, we examined the genomic content and functional potential of Ferrovales in publicly available metagenomic data sets. Our analysis uncovered several new species of Ferrovales as well as an expanded metabolic potential for this group. Comparative genomics suggests that functional diversity may lead to the co-occurrence of multiple Ferrovales species. The presence of multiple iron-oxidizing taxa with distinct physiology could be beneficial for bioremediation strategies.