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Metagenomics-guided analysis of microbial chemolithoautotrophic phosphite oxidation yields evidence of a seventh natural CO2 fixation pathway

  1. John D. Coatesa,2
  1. aDepartment of Plant and Microbial Biology, University of California, Berkeley, CA 94720
  1. Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved November 2, 2017 (received for review September 5, 2017)

Significance

Phosphite (HPO32?) is the most energetically favorable biological electron donor known, but only one organism capable of growing by phosphite oxidation has been previously identified. Here, we describe a phosphite-oxidizing bacterium that can grow with CO2 as its sole electron acceptor, and we propose a metabolic model in which inorganic carbon is assimilated via the reductive glycine pathway. Although the reductive glycine pathway has previously been identified as a “synthetic” carbon fixation pathway, this study provides evidence that it may actually function as a natural autotrophic pathway. Our results suggest that phosphite may serve as a driver of microbial growth and carbon fixation in energy-limited environments, particularly in aphotic environments lacking alternative terminal electron acceptors.

Abstract

Dissimilatory phosphite oxidation (DPO), a microbial metabolism by which phosphite (HPO32?) is oxidized to phosphate (PO43?), is the most energetically favorable chemotrophic electron-donating process known. Only one DPO organism has been described to date, and little is known about the environmental relevance of this metabolism. In this study, we used 16S rRNA gene community analysis and genome-resolved metagenomics to characterize anaerobic wastewater treatment sludge enrichments performing DPO coupled to CO2 reduction. We identified an uncultivated DPO bacterium, Candidatus Phosphitivorax (Ca. P.) anaerolimi strain Phox-21, that belongs to candidate order GW-28 within the Deltaproteobacteria, which has no known cultured isolates. Genes for phosphite oxidation and for CO2 reduction to formate were found in the genome of Ca. P. anaerolimi, but it appears to lack any of the known natural carbon fixation pathways. These observations led us to propose a metabolic model for autotrophic growth by Ca. P. anaerolimi whereby DPO drives CO2 reduction to formate, which is then assimilated into biomass via the reductive glycine pathway.

Footnotes

  • ?1Present address: Institute for Microbiology, ETH Zürich, Zürich, Switzerland.

  • ?2To whom correspondence should be addressed. Email: jdcoates{at}berkeley.edu.
  • Author contributions: I.A.F. and J.D.C. designed research; I.A.F. and P.Y.S. performed research; T.P.B., C.I.C., and A.L.E. contributed new reagents/analytic tools; I.A.F. and J.D.C. analyzed data; and I.A.F., T.P.B., A.L.E., and J.D.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The full 16S rRNA gene sequence of Ca. Phosphitivorax anaerolimi Phox-21 has been deposited in the GenBank (GB) database (accession no. KU898264). MiSeq reads from community 16S rRNA gene amplicon sequencing have been deposited in the National Center for Biotechnology Information Sequence Read Archive (accession no. SRP071909). The combined metagenomic assembly of all four enrichment community samples has been deposited in the Integrated Microbial Genomes (IMG) database (accession no. Ga0100964). Individual genomes recovered from the combined assembly are available in the IMG and GB databases under the following accession nos.: Ca. Phosphitivorax anaerolimi Phox-21, Ga0115057 (IMG), MPOS00000000 (GB); Tepidanaerobacter sp. EBM-38, Ga0115060 (IMG), MPOT00000000 (GB); unclassified bacterium EBM-40, Ga0115061 (IMG), MPOU00000000 (GB); Proteiniphilum sp. EBM-39, Ga0115062 (IMG), MPOV00000000 (GB); Thermotogales bacterium EBM-19, Ga0115064 (IMG), MPOW00000000 (GB); Proteiniphilum sp. EBM-41, Ga0115065 (IMG), MPOX00000000 (GB); Methanoculleus sp. EBM-46, Ga0115067 (IMG), MPOY00000000 (GB); Coprothermobacter sp. EBM-25, Ga0115069 (IMG), MPOZ00000000 (GB); Methanococcoides sp. EBM-47, Ga0115071 (IMG), MPPA00000000 (GB); Spirochaeta sp. EBM-43, Ga0115073 (IMG), MPPB00000000 (GB); Aminobacterium sp. EBM-42, Ga0115070 (IMG), MPPC00000000 (GB); Thermotogales bacterium EBM-38, Ga0115076 (IMG), MPPD00000000 (GB); Tepidanaerobacter sp. EBM-49, Ga0115075 (IMG), MPPE00000000 (GB).

  • This article contains supporting information online at www.danielhellerman.com/lookup/suppl/doi:10.1073/pnas.1715549114/-/DCSupplemental.

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