Dr. John Peters

John Peters

509-335-3412
jw.peters@wsu.edu
Professor and Director, Institute of Biological Chemistry, Ph.D. 1995, Virginia Tech

 John Peters.

RESEARCH

Biological electron transfer reactions are of paramount importance in the metabolism.  My research focuses on the study of the fundamental electron transfer reactions in biology that are relevant to energy and agriculture. The lab uses a variety of different approaches to examine the ecology, physiology, and biochemistry of pathways and reactions that involve oxidation-reduction reactions.

The availability of fixed nitrogen limits global nutrition. We study the process of biological nitrogen fixation that occurs in diverse groups of microorganisms and is an enzymatic process by which atmospheric nitrogen is converted to ammonia.  Through structural and spectroscopic work we study the catalytic mechanism of the enzyme nitrogenase that catalyzes this process. We are also involved in examining redox and energy homeostasis and regulation in model nitrogen fixing organisms and engineering microorganisms to express high levels of the enzymes and excrete ammonia.  This work is aimed in the long term to reduce our dependency on the use of nitrogenous fertilizers in agriculture.

Energy can be stored in H-H, C-H, or N-H bonds and fuel compounds having these bonds can be produced in all forms of life through electron transfer reactions.  We are examining the fundamentals of biological electron reactions as it relates to control of electron flow in organisms to enhance biofuel production.

 

PUBLICATIONS

J.W. Peters, D.N. Beratan, B. Bothner, R.B Dyer, C.S. Harwood, Z.M. Heiden, R. Hille, A.K. Jones, P.W. King, Y. Lu, C.E. Lubner, S.D. Minteer, D.W. Mulder, S. Raugei, G.J. Schut, L.C. Seefeldt, M. Tokmina-Lukaszewska, O. Zadvornyy, P. Zhang, M.W. W. Adams “A new era for electron bifurcation” Curr. Opin. Chem. Biol. 47:32-28 (2018)

L.C. Seefeldt, J.W. Peters, D.N. Beratan, B. Bothner, S.D. Minteer, S. Raugei, and B.M. Hoffman “Control of electron transfer in nitrogenase” Curr. Opin. Chem. Biol. 47:54-59 (2018)

L.C. Seefeldt, B.M. Hoffman, J.W. Peters, S. Raugei, D.N. Beratan, E. Antony, D.R. Dean “Energy transduction in nitrogenase” Acc. Chem. Res. 51-2179-2186 (2018)

J.W. Peters, D.N. Beratan, G.J. Schut, M.W.W. Adams “On the nature of organic and inorganic centers that bifurcate electrons, coupling exergonic and endergonic oxidation-reduction reactions” Chem. Commun. 54:4091-4099 (2018)

S.M. Keable, O.A. Zadvornyy, L. Johnson, B. Ginovska, A.J. Rasmussen, K. Danyal, B.J. Eilers, G.A. Prussia, A.X. LeVan, S. Raugei, L.C. Seefeldt. J.W. Peters “Characterization of the P1+ intermediate state of nitrogenase P-cluster” J. Biol. Chem. 293:9629-9635 (2018)

Mus, A.B. Alleman, N. Pence, J.W. Peters “Exploring the alternatives of biological nitrogen fixation” Metallomics 10:523-528 (2018)

Yu, C.-H. Wu, G.J. Schut, G. Zhao, J.W. Peters, M.W. W. Adams, Huilin Li “Structure of an Ancient Respiratory System” Cell 173:1636-1649 (2018)

Poudel, D.R. Colman, K.R. Fixen, R.N. Ledbetter, Y. Zheng, N. Pence, J.W. Peters, L.C. Seefeldt, C.S. Harwood, E.S. BoydElectron transfer to nitrogenase in different genomic and metabolic backgrounds” J. Bacteriol. pii: JB.00757-17. doi: 10.1128/JB.00757-17 (2018)

Berry, A. Patterson, N. Pence, J.W. Peters, B. Bothner “Hydrogen deuterium exchange mass spectrometry of oxygen sensitive proteins” Bio-protocol pii: e2769. doi: 10.21769/BioProtoc.2769 (2018)

H.D. Duan, C.E. Lubner, M. Tokmina-Lukaszewska, G.H. Gauss, B. Bothner, P.W. King, J.W. Peters, A-F. Miller “Distinct flavin properties underlie flavin-based electron bifurcation within a novel electron transfer flavoprotein FixAB from Rhodopseudomonas palustrisJ. Biol. Chem. 293:4688-4701 (2018)

S.E. Partovi, F. Mus, A.E. Gutknecht, H.A. Martinez, B.P. Tripet, B.M. Lange, J.L. DuBois, J.W. Peters “Coenzyme M biosynthesis in bacteria involves phosphate elimination by a unique member of the aspartase/fumarase superfamily” J. Biol. Chem. 293:5236-5246 (2018)

S.M. Keable, J. Vertemara, O.A. Zadvornyy, B.J. Eilers, K. Danyal, A.J. Rasmussen, L. De Gioia, G. Zampella, L.C. Seefeldt, J.W. Peters “Structural characterization of the nitrogenase MoFe protein with the substrate acetylene trapped near the active site” J. Inorg. Biochem. 180:129-134 (2018)

Berry, S. Poudel, M. Tokmina-Lukaszewska, D. Colman, G.J. Schut, M.W. W. Adams, J.W. Peters, E.S. Boyd, B. Bothner. “H/D Exchange mass spectrometry and statistical coupling analysis reveal a role for allostery in a transhydrogenase catalytic cycle” Biochim. Biophys. Acta-GS 1862(1):9-17 (2018)

C.E. Lubner and J.W. Peters “Electron bifurcation makes the puzzle pieces fall energetically into place in methanogenic energy conservation” ChemBioChem 18:2295-2297. (2017)

Zhang, J.L. Yuly, C.E. Lubner, D.W. Mulder, P.W. King, J.W. Peters, D.N. Beratan. “Electron bifurcation: Thermodynamics and kinetics of multi-electron brokering in biological redox chemistry” Acc. Chem. Res. 50:2410-2417 (2017)

Garcia-Costas, S. Poudel, A-F. Miller, G.J. Schut, R.N. Ledbetter, K. Fixen, L.C. Seefeldt, M.W.W. Adams, C.S. Harwood, E.S. Boyd, J.W. Peters. “Defining electron bifurcation in the electron transferring flavoprotein Family” J. Bacteriol. 199(21) (2017)

Losey, F. Mus, J.W. Peters, H. Le, M. McInerney. “Syntrophomonas wolfeiUses a NADH-dependent, ferredoxin-independent, [FeFe]-hydrogenase to reoxidize NADH” Appl. Environ. Microbiol. 83(20) (2017)

J.H. Artz, O.A. Zadvornyy, D.W. Mulder, P.W. King, J.W. Peters. “Structural characterization of poised states in the oxygen sensitive hydrogenases and nitrogenases” Meth. in Enzymol. 595:213-259 (2017)

B.M. Barney, M.H. Plunkett, V. Natarajan, F. Mus, J.W. Peters. “Transcriptional analysis of an ammonium-excreting strain of Azotobacter vinelandii deregulated for nitrogen fixation” App. Environ. Microbiol. 83(20) (2017)

N. Pence, M. Tokmina-Lukaszewska, Z-Y. Yang, R.N. Ledbetter, L.C. Seefeldt, B. Bothner, J.W. Peters. “Interactions between Fe protein and flavodoxin support reduction preceding nucleotide exchange in the nitrogenase Fe protein cycle” J. Biol. Chem. 292:15661-15669 (2017)

D.M.N. Nguyen, G.J. Schut, S. Poudel, O.A. Zadvornyy, M. Tokmina-Lukaszewska, G.L. Lipscomb, L.A. Adams, J. Dimsmore, W. Nixon, B. Bothner, E.S. Boyd, J.W. Peters, M.W.W. Adams, “Two Functionally distinct bifurcating NADP-dependent ferredoxin oxidoreductases maintain the primary redox balance of Pyrococcus furiosusJ. Biol. Chem. 292:14603-14616 (2017)

Mus, B.J. Eilers, A.B. Alleman, B.V. Kabasakal, J.N. Wells, J.W. Murray, B.P. Nocek, J.L. DuBois, J.W. Peters. “Structural basis for the mechanism of ATP-dependent acetone carboxylation”  Nat. Sci. Rep. 7:7234. (2017)

R.N. Ledbetter, A.M. Garcia Costas, C.E. Lubner, D.W. Mulder, M. Tokmina-Lukaszewska, J.H. Artz, A.  Patterson, T.S. Magnuson, Z.J.H Jay, D. Duan, J. Miller, M.H. Plunkett, J.P. Hoben, B.M. Barney, R.P. Carlson, A-F. Miller, B. Bothner, P.W. King, J.W. Peters, Peters, L.C. Seefeldt. “The electron bifurcating FixABCX protein complex from Azotobacter vinelandii: Generation of low-potential reducing equivalents for nitrogenase catalysis” Biochemistry 56:4177-4190 (2017)

J.H. Artz, D.W. Mulder, S. Poudel, D. Colman, G.J. Schut, S.G. Williams, A.K. Jones, M.W.W. Adams, E.S. Boyd, P.W. King, J.W. Peters. “Structure-function of [FeFe]- and [NiFe]-hydrogenases: An overview of diversity, mechanism, maturation, and bifurcation” Book chapter in “Microalgal Hydrogen Production: Achievements and Prospectives” Eds. G. Torzillo and M. Seibert, Royal Society of Chemistry (2017)

M.J. Amenabar, E.L. Shock, E.E. Roden, J.W. Peters, E.S. Boyd. “Energy demand, not supply, dictates microbial substrate preference” Nat. Geosci. 10:577-581 (2017)

J.H. Artz, D.W. Mulder, M.W. Ratzloff, C.E. Lubner, O.A. Zadvornyy, A.X. LeVan, S.G. Williams,

M.W.W. Adams, A.K. Jones, P.W. King, J.W. Peters JW. “Reduction potentials of [FeFe]-hydrogenase accessory iron-sulfur clusters provide insights into the energetics of proton reduction catalysis” J. Am. Chem Soc. 139:9544-9550 (2017)

J.B. Therien, J.H. Artz, S. Poudel, T.L. Hamilton, Z. Liu, S.M. Noone, M.W.W. Adams, P.W. King, D.A. Bryant, E.S. Boyd, J.W. Peters. “The physiological functions and structural determinants of catalytic bias in the [FeFe]-hydrogenases of Clostridium pasteurianum strain W5” Frontiers in Microbiol. 8:1305 (2017)

C.E. Lubner, D.P. Jenning, D.W. Mulder, G.J. Schut, O.A. Zadvornyy, J. Hoben, M. Tokmina-Lukaszewska, L. Berry, D. Nguyen, G.L. Lipscomb, B. Bothner, A.K. Jones, A-F. Miller, P.W. King, M.W.W. Adams, J.W. Peters. “Mechanistic insights into energy conservation by flavin-based electron bifurcation” Nat. Chem. Bio. 13:655-659 (2017)

Mus, A. Tseng, R. Dixon, J.W. Peters. “Diazotrophic growth allows Azotobacter vinelandii to overcome the deleterious effects of a glnE deletion” App. Environ. Micro. 83:13 (2017)

Mus, A. Tseng, R. Dixon, J.W. Peters. “Diazotrophic growth allows Azotobacter vinelandii to overcome the deleterious effects of a glnE deletion” App. Environ. Micro. 83:13 (2017)

Garcia-Costas, D.L. Ragen, J.W. Peters. “Searching for nitrogen-fixing microorganisms using culture-dependent and culture-independent approaches as an original, relevant and successful early research experience” Amer. Biol. Teach. 79:191-197 (2017)

Celis AI, Gauss GH, Streit BR, Shisler K, Moraski GC, Rodgers KR, Lukat-Rodgers GS, Peters JW, DuBois JL. Structure-Based Mechanism for Oxidative Decarboxylation Reactions Mediated by Amino Acids and Heme Propionates in Coproheme Decarboxylase (HemQ). J Am Chem Soc. 2017 Feb 8;139(5):1900-1911. doi: 10.1021/jacs.6b11324.

Prussia GA, Gauss GH, Mus F, Conner L, DuBois JL, Peters JW. Substitution of a conserved catalytic dyad into 2-KPCC causes loss of carboxylation activity. FEBS Lett. 2016 Sep;590(17):2991-6. doi: 10.1002/1873-3468.12325.

Yang ZY, Ledbetter R, Shaw S, Pence N, Tokmina-Lukaszewska M, Eilers B, Guo Q,Pokhrel N, Cash VL, Dean DR, Antony E, Bothner B, Peters JW, Seefeldt LC. Evidence That the Pi Release Event Is the Rate-Limiting Step in the Nitrogenase Catalytic Cycle. Biochemistry. 2016 Jul 5;55(26):3625-35. doi:10.1021/acs.biochem.6b00421.

Poudel S, Tokmina-Lukaszewska M, Colman DR, Refai M, Schut GJ, King PW, Maness PC, Adams MW, Peters JW, Bothner B, Boyd ES. Unification of [FeFe] hydrogenases into three structural and functional groups. Biochim Biophys Acta. 2016 Sep;1860(9):1910-21. doi: 10.1016/j.bbagen.2016.05.034.

Shepard EM, Byer AS, Betz JN, Peters JW, Broderick JB. A Redox Active [2Fe-2S] Cluster on the Hydrogenase Maturase HydF. Biochemistry. 2016 Jun 28;55(25):3514-27. doi: 10.1021/acs.biochem.6b00528.

Brown KA, Harris DF, Wilker MB, Rasmussen A, Khadka N, Hamby H, Keable S, Dukovic G, Peters JW, Seefeldt LC, King PW. Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid. Science. 2016 Apr 22;352(6284):448-50. doi: 10.1126/science.aaf2091.

Mus F, Crook MB, Garcia K, Garcia Costas A, Geddes BA, Kouri ED, Paramasivan P, Ryu MH, Oldroyd GE, Poole PS, Udvardi MK, Voigt CA, Ané JM, Peters JW. Symbiotic Nitrogen Fixation and the Challenges to Its Extension to Nonlegumes.  Appl Environ Microbiol. 2016 Jun 13;82(13):3698-710. doi: 10.1128/AEM.01055-16.

Peters JW, Miller AF, Jones AK, King PW, Adams MW. Electron bifurcation. Curr Opin Chem Biol. 2016 Apr;31:146-52. doi: 10.1016/j.cbpa.2016.03.007. Review.

Schut GJ, Zadvornyy O, Wu CH, Peters JW, Boyd ES, Adams MW. The role of geochemistry and energetics in the evolution of modern respiratory complexes from a proton-reducing ancestor. Biochim Biophys Acta. 2016 Jul;1857(7):958-70. doi: 10.1016/j.bbabio.2016.01.010. Review.

Artz JH, White SN, Zadvornyy OA, Fugate CJ, Hicks D, Gauss GH, Posewitz MC, Boyd ES, Peters JW. Biochemical and Structural Properties of a Thermostable Mercuric Ion Reductase from Metallosphaera sedula. Front Bioeng Biotechnol. 2015 Jul 13;3:97. doi: 10.3389/fbioe.2015.00097. PubMed PMID: 26217660;

Zadvornyy OA, Boyd ES, Posewitz MC, Zorin NA, Peters JW. Biochemical and Structural Characterization of Enolase from Chloroflexus aurantiacus: Evidence for a Thermophilic Origin. Front Bioeng Biotechnol. 2015 Jun 1;3:74. doi: 10.3389/fbioe.2015.00074. PubMed PMID: 26082925;

Danyal K, Rasmussen AJ, Keable SM, Inglet BS, Shaw S, Zadvornyy OA, Duval S, Dean DR, Raugei S, Peters JW, Seefeldt LC. Fe protein-independent substrate reduction by nitrogenase MoFe protein variants. Biochemistry. 2015 Apr 21;54(15):2456-62. doi: 10.1021/acs.biochem.5b00140.

Urschel MR, Kubo MD, Hoehler TM, Peters JW, Boyd ES. Carbon source preference in chemosynthetic hot spring communities. Appl Environ Microbiol. 2015 Jun;81(11):3834-47. doi: 10.1128/AEM.00511-15.

Betz JN, Boswell NW, Fugate CJ, Holliday GL, Akiva E, Scott AG, Babbitt PC, Peters JW, Shepard EM, Broderick JB. [FeFe]-hydrogenase maturation: insights into the role HydE plays in dithiomethylamine biosynthesis. Biochemistry. 2015 Mar 10;54(9):1807-18. doi: 10.1021/bi501205e. PubMed PMID: 25654171;

Boyd ES, Costas AM, Hamilton TL, Mus F, Peters JW. Evolution of molybdenum nitrogenase during the transition from anaerobic to aerobic metabolism. J Bacteriol. 2015 May;197(9):1690-9. doi: 10.1128/JB.02611-14. 25733617; PubMed Central PMCID:

Geddes BA, Ryu MH, Mus F, Garcia Costas A, Peters JW, Voigt CA, Poole P. Use of plant colonizing bacteria as chassis for transfer of N₂-fixation to cereals. Curr Opin Biotechnol. 2015 Apr;32:216-22. doi: 10.1016/j.copbio.2015.01.004.

Swanson KD, Ratzloff MW, Mulder DW, Artz JH, Ghose S, Hoffman A, White S, Zadvornyy OA, Broderick JB, Bothner B, King PW, Peters JW. [FeFe]-hydrogenase oxygen inactivation is initiated at the H cluster 2Fe subcluster. J Am Chem Soc. 2015 Feb 11;137(5):1809-16. doi: 10.1021/ja510169s.

Byer AS, Shepard EM, Peters JW, Broderick JB. Radical S-adenosyl-L-methionine chemistry in the synthesis of hydrogenase and nitrogenase metal cofactors. J Biol Chem. 2015 Feb 13;290(7):3987-94. doi: 10.1074/jbc.R114.578161

Boyd ES, Hamilton TL, Swanson KD, Howells AE, Baxter BK, Meuser JE, Posewitz MC, Peters JW. [FeFe]-hydrogenase abundance and diversity along a vertical redox  gradient in Great Salt Lake, USA. Int J Mol Sci. 2014 Nov 28;15(12):21947-66. doi: 10.3390/ijms151221947.

Peters JW, Schut GJ, Boyd ES, Mulder DW, Shepard EM, Broderick JB, King PW, Adams MW. [FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation. Biochim Biophys Acta. 2015 Jun;1853(6):1350-69. doi: 10.1016/j.bbamcr.2014.11.021.

Cohen AE, Soltis SM, González A, Aguila L, Alonso-Mori R, Barnes CO, Baxter EL, Brehmer W, Brewster AS, Brunger AT, Calero G, Chang JF, Chollet M, Ehrensberger P, Eriksson TL, Feng Y, Hattne J, Hedman B, Hollenbeck M, Holton JM, Keable S, Kobilka BK, Kovaleva EG, Kruse AC, Lemke HT, Lin G, Lyubimov AY, Manglik A, Mathews II, McPhillips SE, Nelson S, Peters JW, Sauter NK, Smith CA, Song J, Stevenson HP, Tsai Y, Uervirojnangkoorn M, Vinetsky V, Wakatsuki S, Weis WI, Zadvornyy OA, Zeldin OB, Zhu D, Hodgson KO. Goniometer-based femtosecond crystallography with X-ray free electron lasers. Proc Natl Acad Sci U S A. 2014 Dec 2;111(48):17122-7. doi: 10.1073/pnas.1418733111.