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The Diversity and Evolution of Microbial Dissimilatory Phosphite Oxidation

Sophia D. Ewens, Alexa F. S. Gomberg, Tyler P. Barnum, Mikayla A. Borton, Hans K. Carlson, Kelly C. Wrighton, John D. Coates
doi: https://doi.org/10.1101/2020.12.28.424620
Sophia D. Ewens
1Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA
2Energy & Biosciences Institute, University of California, Berkeley, CA, USA
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Alexa F. S. Gomberg
1Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA
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Tyler P. Barnum
1Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA
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Mikayla A. Borton
4Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO, USA
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Hans K. Carlson
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Lab, Berkeley, CA, USA
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Kelly C. Wrighton
4Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO, USA
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John D. Coates
1Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA
2Energy & Biosciences Institute, University of California, Berkeley, CA, USA
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  • For correspondence: jdcoates@berkeley.edu
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Abstract

Phosphite is the most energetically favorable chemotrophic electron donor known, with a half-cell potential (E°’) of −650 mV for the PO4 3-/PO3 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 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.

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.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
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Posted December 28, 2020.
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The Diversity and Evolution of Microbial Dissimilatory Phosphite Oxidation
Sophia D. Ewens, Alexa F. S. Gomberg, Tyler P. Barnum, Mikayla A. Borton, Hans K. Carlson, Kelly C. Wrighton, John D. Coates
bioRxiv 2020.12.28.424620; doi: https://doi.org/10.1101/2020.12.28.424620
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The Diversity and Evolution of Microbial Dissimilatory Phosphite Oxidation
Sophia D. Ewens, Alexa F. S. Gomberg, Tyler P. Barnum, Mikayla A. Borton, Hans K. Carlson, Kelly C. Wrighton, John D. Coates
bioRxiv 2020.12.28.424620; doi: https://doi.org/10.1101/2020.12.28.424620

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