The diversity and evolution of microbial dissimilatory phosphite oxidation
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Abstract
Abstract Phosphite is the most energetically favorable chemotrophic electron donor known, with a half-cell potential (E°’) of −650 mV for the PO 4 3- /PO 3 3- couple. Since the discovery of microbial dissimilatory phosphite oxidation (DPO) in 2000, the environmental distribution, evolution, and diversity of DPO microorganisms (DPOM) has remained enigmatic and only two species have been identified. Here metagenomic sequencing of phosphite enriched microbial communities enabled the reconstruction and metabolic characterization of 21 novel DPOM. These DPOM 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 to 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 CO 2 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. Significance Statement 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 Earth’s history and continue to do so in contemporary environments.
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Phosphite oxidation genes are commonplace today, being found in roughly 1.5% of all genomes.
“But phosphite oxidation genes are commonplace today (Schink and Friedrich, 2000; Vrtis et al., 2001), being found in roughly 1.5 % of all genomes (Ewens et al., 2021)”
From Serpentinization as the source of energy, electrons, organics, catalysts, nutrients and pH gradients for the origin of LUCA and life (2023) · cites this paper as Ewens et al., 2021
The Main Text Introduction (page not available) gives the roughly 1.5% figure, but says functional genes predict that phosphite is assimilated as a phosphorus source by approximately 1.5% of sequenced microorganisms. It does not establish that phosphite-oxidation genes occur in 1.5% of all genomes, or that the figure applies specifically to dissimilatory phosphite oxidation. (LLM, conf=0.88)
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AMP-dependent phosphite dehydrogenase, a phosphorylating enzyme in dissimilatory phosphite oxidation
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Ignored effects of phosphite (P+III) on the growth responses of three typical algae species
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Evolution of phosphate scouting in the terrestrial biosphere
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Evaluating Serpentinization as a Source of Phosphite to Microbial Communities in Hydrothermal Vents
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Widespread promiscuous alkaline phosphatases underscore ancient microbial phosphite utilization
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Hypophosphite Is a Naturally Occurring Selective Inhibitor of Syntrophic Methanogenesis
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Can Phosphite Substitute for Phosphate in ptxD Rice? Evidence From Uptake and Agronomic Performance
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Solar–Chemical Hybrid‐Driven Phototroph for Biosynthesis
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- Authors
- Ewens, S. D., Gomberg, A. F. S., Barnum, T. P., Borton, M. A., Carlson, H. K., Wrighton, K. C., & Coates, J. D.
- Affiliations
- Energy Biosciences Institute (US)
- University of California, Berkeley (US)
- Colorado State University (US)
- Lawrence Berkeley National Laboratory (US)
- Corresponding author
- Coates, John D.
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2021-03-09
- Volume
- 118
- Issue
- 11
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC7980464
- OpenAlex
- W3135509950
- Cited by
- 48
- References
- 82
- Citations by year
- 2026: 13 · 2025: 10 · 2024: 8 · 2023: 12 · 2022: 3 · 2021: 2
- FWCI
- 3.37
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- Funders
- Energy Biosciences Institute (H5940)
- U.S. Department of Energy (DE-SC0020156)
- Topics
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
- Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
- Keywords
- phosphorus cycling, phosphites, autotrophic bacteria, anoxia, microbial energy metabolism, phosphate availability, redox cycling, bioavailable phosphorus
- MeSH terms
- Anaerobiosis, Bacteria, Bacterial Proteins, Carbon Dioxide, Energy Metabolism, Oxidation-Reduction, Phylogeny, Genetic Variation, Genome, Bacterial, Phosphites, Evolution, Molecular, Biodiversity, Chemoautotrophic Growth, Wastewater, Microbiota
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