The diversity and evolution of microbial dissimilatory phosphite oxidation

Ewens, Sophia D.; Gomberg, Alexa S.; Barnum, Tyler P.; Borton, Mikayla A.; Carlson, Hans K.; Wrighton, Kelly C.; Coates, John D.

doi:10.1073/pnas.2020024118

Title: The diversity and evolution of microbial dissimilatory phosphite oxidation

Journal Article · 09 March 2021 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.2020024118 · OSTI ID:1770007

^[1];

^[1]; Barnum, Tyler P. ^[1]; Borton, Mikayla A. ^[2];

^[3];

^[2]; Coates, John D. ^[4]

Univ. of California, Berkeley, CA (United States)
Colorado State Univ., Fort Collins, CO (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Phosphite is the most energetically favorable chemotrophic electron donor known, with a half-cell potential (E^o') 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 (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 me tabolism 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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231; SC0020156

OSTI ID:: 1770007

Alternate ID(s):: OSTI ID: 1844521

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 118, Issue 11; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (68)

Investigation of schreibersite and intrinsic oxidation products from Sikhote-Alin, Seymchan, and Odessa meteorites and Fe3P and Fe2NiP synthetic surrogates Pirim, C.; Pasek, M. A.; Sokolov, D. A. Geochimica et Cosmochimica Acta, Vol. 140 https://doi.org/10.1016/j.gca.2014.05.027	journal	September 2014
Metagenomics-guided analysis of microbial chemolithoautotrophic phosphite oxidation yields evidence of a seventh natural CO ₂ fixation pathway Figueroa, Israel A.; Barnum, Tyler P.; Somasekhar, Pranav Y. Proceedings of the National Academy of Sciences, Vol. 115, Issue 1 https://doi.org/10.1073/pnas.1715549114	journal	November 2017
Anvi’o: an advanced analysis and visualization platform for ‘omics data Eren, A. Murat; Esen, Özcan C.; Quince, Christopher PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1319	journal	January 2015
DRAM for distilling microbial metabolism to automate the curation of microbiome function Shaffer, Michael; Borton, Mikayla A.; McGivern, Bridget B. Nucleic Acids Research, Vol. 48, Issue 16 https://doi.org/10.1093/nar/gkaa621	journal	August 2020
Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas Nature Biotechnology, Vol. 35, Issue 8 https://doi.org/10.1038/nbt.3893	journal	August 2017
Decoupled genomic elements and the evolution of partner quality in nitrogen‐fixing rhizobia Gordon, Benjamin R.; Klinger, Christie R.; Weese, Dylan J. Ecology and Evolution, Vol. 6, Issue 5 https://doi.org/10.1002/ece3.1953	journal	January 2016
A survey of carbon fixation pathways through a quantitative lens Bar-Even, Arren; Noor, Elad; Milo, Ron Journal of Experimental Botany, Vol. 63, Issue 6, p. 2325-2342 https://doi.org/10.1093/jxb/err417	journal	December 2011
Desulfotignum phosphitoxidans sp. nov., a new marine sulfate reducer that oxidizes phosphite to phosphate Schink, Bernhard; Thiemann, Volker; Laue, Heike Archives of Microbiology, Vol. 177, Issue 5 https://doi.org/10.1007/s00203-002-0402-x	journal	May 2002
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
Phosphite in Sedimentary Interstitial Water of Lake Taihu, a Large Eutrophic Shallow Lake in China Han, Chao; Geng, Jinju; Ren, Hongqiang Environmental Science & Technology, Vol. 47, Issue 11 https://doi.org/10.1021/es305297y	journal	May 2013
Identification and Heterologous Expression of Genes Involved in Anaerobic Dissimilatory Phosphite Oxidation by Desulfotignum phosphitoxidans Simeonova, D. D.; Wilson, M. M.; Metcalf, W. W. Journal of Bacteriology, Vol. 192, Issue 19 https://doi.org/10.1128/JB.00541-10	journal	July 2010
Determination of phosphite in a full-scale municipal wastewater treatment plant Yu, Xiaolong; Geng, Jinju; Ren, Hongqiang Environmental Science: Processes & Impacts, Vol. 17, Issue 2 https://doi.org/10.1039/C4EM00543K	journal	January 2015
Rethinking early Earth phosphorus geochemistry Pasek, M. A. Proceedings of the National Academy of Sciences, Vol. 105, Issue 3 https://doi.org/10.1073/pnas.0708205105	journal	January 2008
Ultrafast clustering algorithms for metagenomic sequence analysis Li, W.; Fu, L.; Niu, B. Briefings in Bioinformatics, Vol. 13, Issue 6 https://doi.org/10.1093/bib/bbs035	journal	July 2012
Biological formation of volatile phosphorus compounds Roels, Joris; Verstraete, Willy Bioresource Technology, Vol. 79, Issue 3 https://doi.org/10.1016/S0960-8524(01)00032-3	journal	September 2001
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Li, Dinghua; Liu, Chi-Man; Luo, Ruibang Bioinformatics, Vol. 31, Issue 10 https://doi.org/10.1093/bioinformatics/btv033	journal	January 2015
“Unknown Genome” Proteomics Simeonova, Diliana Dancheva; Susnea, Iuliana; Moise, Adrian Molecular & Cellular Proteomics, Vol. 8, Issue 1 https://doi.org/10.1074/mcp.M800242-MCP200	journal	January 2009
One-Step Treatment of Phosphite-Laden Wastewater: A Single Electrochemical Reactor Integrating Superoxide Radical-Induced Oxidation and Electrocoagulation Liang, Sheng; Zheng, Wenxiao; Zhu, Liuyi Environmental Science & Technology, Vol. 53, Issue 9 https://doi.org/10.1021/acs.est.9b00841	journal	April 2019
EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data Miller, Christopher S.; Baker, Brett J.; Thomas, Brian C. Genome Biology, Vol. 12, Issue 5 https://doi.org/10.1186/gb-2011-12-5-r44	journal	May 2011
Redox chemistry in the phosphorus biogeochemical cycle Pasek, M. A.; Sampson, J. M.; Atlas, Z. Proceedings of the National Academy of Sciences, Vol. 111, Issue 43 https://doi.org/10.1073/pnas.1408134111	journal	October 2014
Lightning-induced reduction of phosphorus oxidation state Pasek, Matthew; Block, Kristin Nature Geoscience, Vol. 2, Issue 8 https://doi.org/10.1038/ngeo580	journal	July 2009
Hidden Markov model speed heuristic and iterative HMM search procedure Johnson, L. Steven; Eddy, Sean R.; Portugaly, Elon BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-431	journal	August 2010
Centrifuge: rapid and sensitive classification of metagenomic sequences Kim, Daehwan; Song, Li; Breitwieser, Florian P. Genome Research, Vol. 26, Issue 12 https://doi.org/10.1101/gr.210641.116	journal	October 2016
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Phosphite oxidation by sulphate reduction Schink, Bernhard; Friedrich, Michael Nature, Vol. 406, Issue 6791 https://doi.org/10.1038/35017644	journal	July 2000
The Genome Portal of the Department of Energy Joint Genome Institute Grigoriev, I. V.; Nordberg, H.; Shabalov, I. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr947	journal	November 2011
Evidence for reactive reduced phosphorus species in the early Archean ocean Pasek, M. A.; Harnmeijer, J. P.; Buick, R. Proceedings of the National Academy of Sciences, Vol. 110, Issue 25 https://doi.org/10.1073/pnas.1303904110	journal	June 2013
Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae) Li, Gang; Davis, Brian W.; Eizirik, Eduardo Genome Research, Vol. 26, Issue 1 https://doi.org/10.1101/gr.186668.114	journal	October 2015
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
In Vivo Assimilation of One-Carbon via a Synthetic Reductive Glycine Pathway in Escherichia coli Yishai, Oren; Bouzon, Madeleine; Döring, Volker ACS Synthetic Biology, Vol. 7, Issue 9 https://doi.org/10.1021/acssynbio.8b00131	journal	May 2018
Characterization of the anaerobic propionate-degrading syntrophs Smithella propionica gen. nov., sp. nov. and Syntrophobacter wolinii Liu, Yitai; Balkwill, David L.; Aldrich, Henry C. International Journal of Systematic and Evolutionary Microbiology, Vol. 49, Issue 2 https://doi.org/10.1099/00207713-49-2-545	journal	April 1999
Genome-based taxonomic framework for the class Negativicutes: division of the class Negativicutes into the orders Selenomonadales emend., Acidaminococcales ord. nov. and Veillonellales ord. nov. Campbell, Chantal; Adeolu, Mobolaji; Gupta, Radhey S. International Journal of Systematic and Evolutionary Microbiology, Vol. 65, Issue 9 https://doi.org/10.1099/ijs.0.000347	journal	September 2015
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Earth's Phosphides in Levant and insights into the source of Archean prebiotic phosphorus Britvin, Sergey N.; Murashko, Michail N.; Vapnik, Yevgeny Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep08355	journal	February 2015
Physiology, Ecology, Phylogeny, and Genomics of Microorganisms Capable of Syntrophic Metabolism McInerney, Michael J.; Struchtemeyer, Christopher G.; Sieber, Jessica Annals of the New York Academy of Sciences, Vol. 1125, Issue 1 https://doi.org/10.1196/annals.1419.005	journal	March 2008
Syntrophy in anaerobic global carbon cycles McInerney, Michael J.; Sieber, Jessica R.; Gunsalus, Robert P. Current Opinion in Biotechnology, Vol. 20, Issue 6 https://doi.org/10.1016/j.copbio.2009.10.001	journal	December 2009
KEGG as a reference resource for gene and protein annotation Kanehisa, Minoru; Sato, Yoko; Kawashima, Masayuki Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1070	journal	October 2015
Purification and Characterization of a Novel Phosphorus-oxidizing Enzyme from Pseudomonas stutzeri WM88 Costas, Amaya M. Garcia; White, Andrea K.; Metcalf, William W. Journal of Biological Chemistry, Vol. 276, Issue 20 https://doi.org/10.1074/jbc.M011764200	journal	February 2001
Desulfomonile tiedjei gen. nov. and sp. nov., a novel anaerobic, dehalogenating, sulfate-reducing bacterium DeWeerd, KimA.; Mandelco, Linda; Tanner, RalphS. Archives of Microbiology, Vol. 154, Issue 1 https://doi.org/10.1007/BF00249173	journal	June 1990
Formate Assimilation: The Metabolic Architecture of Natural and Synthetic Pathways Bar-Even, Arren Biochemistry, Vol. 55, Issue 28 https://doi.org/10.1021/acs.biochem.6b00495	journal	July 2016
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
SimpleSynteny: a web-based tool for visualization of microsynteny across multiple species Veltri, Daniel; Wight, Martha Malapi; Crouch, Jo Anne Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw330	journal	May 2016
Systematic Identification of Gene Families for Use as “Markers” for Phylogenetic and Phylogeny-Driven Ecological Studies of Bacteria and Archaea and Their Major Subgroups Wu, Dongying; Jospin, Guillaume; Eisen, Jonathan A. PLoS ONE, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pone.0077033	journal	October 2013
AnnoTree: visualization and exploration of a functionally annotated microbial tree of life Mendler, Kerrin; Chen, Han; Parks, Donovan H. Nucleic Acids Research, Vol. 47, Issue 9 https://doi.org/10.1093/nar/gkz246	journal	April 2019
Cyclohexane Carboxylate and Benzoate Formation from Crotonate in Syntrophus aciditrophicus Mouttaki, H.; Nanny, M. A.; McInerney, M. J. Applied and Environmental Microbiology, Vol. 73, Issue 3 https://doi.org/10.1128/AEM.02227-06	journal	December 2006
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB Pruesse, E.; Quast, C.; Knittel, K. Nucleic Acids Research, Vol. 35, Issue 21 https://doi.org/10.1093/nar/gkm864	journal	November 2007
Overexpression in Escherichia coli of the rnf genes from Rhodobacter capsulatus . Characterization of two membrane-bound iron-sulfur proteins Jouanneau, Yves; Jeong, Ho-Sang; Hugo, Nicolas European Journal of Biochemistry, Vol. 251, Issue 1-2 https://doi.org/10.1046/j.1432-1327.1998.2510054.x	journal	January 1998
The rise of oxygen in Earth’s early ocean and atmosphere Lyons, Timothy W.; Reinhard, Christopher T.; Planavsky, Noah J. Nature, Vol. 506, Issue 7488 https://doi.org/10.1038/nature13068	journal	February 2014
Genome reduction as the dominant mode of evolution: Prospects & Overviews Wolf, Yuri I.; Koonin, Eugene V. BioEssays, Vol. 35, Issue 9 https://doi.org/10.1002/bies.201300037	journal	June 2013
Binning metagenomic contigs by coverage and composition Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino Nature Methods, Vol. 11, Issue 11 https://doi.org/10.1038/nmeth.3103	journal	September 2014
Dendroscope 3: An Interactive Tool for Rooted Phylogenetic Trees and Networks Huson, Daniel H.; Scornavacca, Celine Systematic Biology, Vol. 61, Issue 6 https://doi.org/10.1093/sysbio/sys062	journal	September 2012
Life based on phosphite: a genome-guided analysis of Desulfotignum phosphitoxidans Poehlein, Anja; Daniel, Rolf; Schink, Bernhard BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-753	journal	January 2013
The reductive glycine pathway allows autotrophic growth of Desulfovibrio desulfuricans Sánchez-Andrea, Irene; Guedes, Iame Alves; Hornung, Bastian Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-18906-7	journal	October 2020
The htx and ptx Operons of Pseudomonas stutzeri WM88 Are New Members of the Pho Regulon White, Andrea K.; Metcalf, William W. Journal of Bacteriology, Vol. 186, Issue 17 https://doi.org/10.1128/JB.186.17.5876-5882.2004	journal	September 2004
Novel syntrophic bacteria in full-scale anaerobic digesters revealed by genome-centric metatranscriptomics Hao, Liping; Michaelsen, Thomas Yssing; Singleton, Caitlin Margaret The ISME Journal, Vol. 14, Issue 4 https://doi.org/10.1038/s41396-019-0571-0	journal	January 2020
Archean phosphorus liberation induced by iron redox geochemistry Herschy, Barry; Chang, Sae Jung; Blake, Ruth Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03835-3	journal	April 2018
Assembly of the Escherichia coli NADH:ubiquinone oxidoreductase (respiratory complex I) Friedrich, Thorsten; Dekovic, Doris Kreuzer; Burschel, Sabrina Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 3 https://doi.org/10.1016/j.bbabio.2015.12.004	journal	March 2016
Methane Biogeochemistry and Methanogen Communities in Two Northern Peatland Ecosystems, New York State Basiliko, N.; Yavitt, J. B.; Dees, P. M. Geomicrobiology Journal, Vol. 20, Issue 6 https://doi.org/10.1080/713851165	journal	November 2003
Hidden Markov Models and their Applications in Biological Sequence Analysis Yoon, Byung-Jun Current Genomics, Vol. 10, Issue 6 https://doi.org/10.2174/138920209789177575	journal	September 2009
Pelotomaculum thermopropionicum gen. nov., sp. nov., an anaerobic, thermophilic, syntrophic propionate-oxidizing bacterium Imachi, H. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 52, Issue 5 https://doi.org/10.1099/ijs.0.02212-0	journal	September 2002
Classification, substrate specificity and structural features of D-2-hydroxyacid dehydrogenases: 2HADH knowledgebase Matelska, Dorota; Shabalin, Ivan G.; Jabłońska, Jagoda BMC Evolutionary Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12862-018-1309-8	journal	December 2018
Crystallographic and kinetic analyses of the FdsBG subcomplex of the cytosolic formate dehydrogenase FdsABG from Cupriavidus necator Young, Tynan; Niks, Dimitri; Hakopian, Sheron Journal of Biological Chemistry, Vol. 295, Issue 19 https://doi.org/10.1074/jbc.RA120.013264	journal	May 2020
Genetic Diversity and Horizontal Transfer of Genes Involved in Oxidation of Reduced Phosphorus Compounds by Alcaligenes faecalis WM2072 Wilson, M. M.; Metcalf, W. W. Applied and Environmental Microbiology, Vol. 71, Issue 1 https://doi.org/10.1128/AEM.71.1.290-296.2005	journal	January 2005
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Microbial Metabolism of Reduced Phosphorus Compounds White, Andrea K.; Metcalf, William W. Annual Review of Microbiology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev.micro.61.080706.093357	journal	October 2007
Synteny footprints provide clearer phylogenetic signal than sequence data for prokaryotic classification Sevillya, Gur; Snir, Sagi Molecular Phylogenetics and Evolution, Vol. 136 https://doi.org/10.1016/j.ympev.2019.03.010	journal	July 2019
The two-domain tree of life is linked to a new root for the Archaea Raymann, Kasie; Brochier-Armanet, Céline; Gribaldo, Simonetta Proceedings of the National Academy of Sciences, Vol. 112, Issue 21 https://doi.org/10.1073/pnas.1420858112	journal	May 2015
A role for phosphorus redox in emerging and modern biochemistry Pasek, Matthew Current Opinion in Chemical Biology, Vol. 49 https://doi.org/10.1016/j.cbpa.2018.09.018	journal	April 2019

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Title: The diversity and evolution of microbial dissimilatory phosphite oxidation

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