The diversity and evolution of microbial dissimilatory phosphite oxidation – pnas.org

Significance

Geochemical models of the phosphorus (P) cycle uniquely ignore microbial redox transformations. Yet phosphite is a reduced P source that has been detected in several environments at concentrations that suggest a contemporary P redox cycle. Microbial dissimilatory phosphite oxidation (DPO) converts soluble phosphite into phosphate, and a false notion of rarity has limited our understanding of its diversity and environmental distribution. Here we demonstrate that DPO is an ancient energy metabolism hosted by taxonomically diverse, autotrophic bacteria that exist globally throughout anoxic environments. DPO microorganisms are therefore likely to have provided bioavailable phosphate and fixed carbon to anoxic ecosystems throughout Earths history and continue to do so in contemporary environments.

Phosphite is the most energetically favorable chemotrophic electron donor known, with a half-cell potential (Eo) of 650 mV for the PO43/PO33 couple. Since the discovery of microbial dissimilatory phosphite oxidation (DPO) in 2000, the environmental distribution, evolution, and diversity of DPO microorganisms (DPOMs) have remained enigmatic, as only two species have been identified. Here, metagenomic sequencing of phosphite-enriched microbial communities enabled the genome reconstruction and metabolic characterization of 21 additional DPOMs. These DPOMs spanned six classes of bacteria, including the Negativicutes, Desulfotomaculia, Synergistia, Syntrophia, Desulfobacteria, and Desulfomonilia_A. Comparing the DPO genes from the genomes of enriched organisms with over 17,000 publicly available metagenomes revealed the global existence of this metabolism in diverse anoxic environments, including wastewaters, sediments, and subsurface aquifers. Despite their newfound environmental and taxonomic diversity, metagenomic analyses suggested that the typical DPOM is a chemolithoautotroph that occupies low-oxygen environments and specializes in phosphite oxidation coupled to CO2 reduction. Phylogenetic analyses indicated that the DPO genes form a highly conserved cluster that likely has ancient origins predating the split of monoderm and diderm bacteria. By coupling microbial cultivation strategies with metagenomics, these studies highlighted the unsampled metabolic versatility latent in microbial communities. We have uncovered the unexpected prevalence, diversity, biochemical specialization, and ancient origins of a unique metabolism central to the redox cycling of phosphorus, a primary nutrient on Earth.

Author contributions: S.D.E. and J.D.C. designed research; S.D.E. and A.F.S.G. performed research; T.P.B., M.A.B., H.K.C., K.C.W., and J.D.C. contributed new reagents/analytic tools; S.D.E., A.F.S.G., and J.D.C. analyzed data; and S.D.E. and J.D.C. wrote the paper.

The authors declare no competing interest.

This article is a PNAS Direct Submission. W.W.M. is a guest editor invited by the Editorial Board.

This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2020024118/-/DCSupplemental.

All metagenomic reads, assemblies, and curated metagenome-assembled genomes reported in this paper (quality metrics >50% complete and <10% redundant) have been deposited in the NCBI BioProject (accession no. PRJNA655520).

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The diversity and evolution of microbial dissimilatory phosphite oxidation - pnas.org