Uncovering hidden phylo- and ecogenomic diversity of the widespread methanotrophic genus <i>Methylobacter</i>

The globally distributed genus Methylobacter plays a crucial role in mitigating methane emissions from diverse ecosystems, including freshwater and marine habitats, wetlands, soils, sediments, groundwater, and landfills. Despite their frequent presence and abundance in these systems, we still know little about the genomic adaptations that they exhibit. Here, we used a collection of 97 genomes and metagenome-assembled genomes to ecogenomically characterize the genus. Our analyses suggest that the genus Methylobacter may contain more species than previously thought, with >30 putative species clusters. Some species clusters shared >98.65% sequence identity of the full-length 16S rRNA gene, demonstrating the need for genome-resolved species delineation. The ecogenomic differences between Methylobacter spp. include various combinations of methane monooxygenases, multigene loci for alternative dissimilatory metabolisms related to hydrogen, sulfur cycling, and denitrification, as well as other lifestyle-associated functions. Additionally, we describe and tentatively name the two new Methylobacter species, which we recently cultured from sediment of a temperate eutrophic fishpond, as Methylobacter methanoversatilis, sp. nov. and Methylobacter spei, sp. nov. Overall, our study highlights previously unrecognized species diversity within the genus Methylobacter, their diverse metabolic potential, versatility, as well as the presence of distinct genomic adaptations for thriving in various environments.