Microbial dissimilatory phosphite oxidation (DPO) is the most energetically favorable chemotrophic microbial metabolism known, with a half cell potential of -650 mV for the phosphate/phosphite couple. The environmental distribution, evolution, and diversity of DPO microorganisms (DPOM) has remained enigmatic for approximately 20 years, as only two species had been identified since the discovery of the metabolism in 2002. Here, we coupled cultivation enrichment strategies to metagenomics, enabling the genomic reconstruction and metabolic characterization of 21 novel DPOM from wastewater treatment sludge. These DPO genomes span six classes of bacteria, including the Negativicutes, Desulfotomaculia, Synergistia, Syntrophia, Desulfobacteria and Desulfomonilia. Comparing the DPO genes from enriched DPO genomes to over 17,000 publicly available metagenomes shows that DPO metabolism exists in diverse anoxic environments worldwide, including wastewaters, sediments, and subsurface aquifers. Despite their newfound environmental and taxonomic diversity, metabolic analyses of DPO MAGs suggest that the typical DPO microorganism is a chemolithoautotroph that specializes in phosphite oxidation and occupies low-oxygen environments. Phylogenetic analyses further indicate that the DPO genes form a highly conserved cluster with ancient origins that predate the split of monoderm and diderm bacteria. By coupling microbial cultivation strategies with metagenomics, we have uncovered DPO lineages that highlight the unsampled metabolic diversity latent in microbial communities, and the genomes we provide here may inspire strategies for obtaining environmental isolates that will be pivotal to advancing our understanding of this unique metabolism.
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