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Perchlorate Reductase Is Distinguished by Active Site Aromatic Gate Residues.

Youngblut MD, Tsai CL, Clark IC, Carlson HK, Maglaqui AP, Gau-Pan PS, Redford SA, Wong A, Tainer JA, Coates JD
J Biol Chem 291 9190-202 (2016)
Related entries: 5ch7, 5chc, 5e7o

Cited: 29 times
EuropePMC logo PMID: 26940877

Abstract

Perchlorate is an important ion on both Earth and Mars. Perchlorate reductase (PcrAB), a specialized member of the dimethylsulfoxide reductase superfamily, catalyzes the first step of microbial perchlorate respiration, but little is known about the biochemistry, specificity, structure, and mechanism of PcrAB. Here we characterize the biophysics and phylogeny of this enzyme and report the 1.86-Å resolution PcrAB complex crystal structure. Biochemical analysis revealed a relatively high perchlorate affinity (Km = 6 μm) and a characteristic substrate inhibition compared with the highly similar respiratory nitrate reductase NarGHI, which has a relatively much lower affinity for perchlorate (Km = 1.1 mm) and no substrate inhibition. Structural analysis of oxidized and reduced PcrAB with and without the substrate analog SeO3 (2-) bound to the active site identified key residues in the positively charged and funnel-shaped substrate access tunnel that gated substrate entrance and product release while trapping transiently produced chlorate. The structures suggest gating was associated with shifts of a Phe residue between open and closed conformations plus an Asp residue carboxylate shift between monodentate and bidentate coordination to the active site molybdenum atom. Taken together, structural and mutational analyses of gate residues suggest key roles of these gate residues for substrate entrance and product release. Our combined results provide the first detailed structural insight into the mechanism of biological perchlorate reduction, a critical component of the chlorine redox cycle on Earth.

Reviews - 4ydd mentioned but not cited (1)

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Articles - 4ydd mentioned but not cited (4)

  1. Perchlorate Reductase Is Distinguished by Active Site Aromatic Gate Residues. Youngblut MD, Tsai CL, Clark IC, Carlson HK, Maglaqui AP, Gau-Pan PS, Redford SA, Wong A, Tainer JA, Coates JD. J Biol Chem 291 9190-9202 (2016)
  2. Synthesis of silver nanoparticles by Bacillus clausii and computational profiling of nitrate reductase enzyme involved in production. Mukherjee K, Gupta R, Kumar G, Kumari S, Biswas S, Padmanabhan P. J Genet Eng Biotechnol 16 527-536 (2018)
  3. Robust Production, Crystallization, Structure Determination, and Analysis of [Fe-S] Proteins: Uncovering Control of Electron Shuttling and Gating in the Respiratory Metabolism of Molybdopterin Guanine Dinucleotide Enzymes. Tsai CL, Tainer JA. Methods Enzymol 599 157-196 (2018)
  4. In Silico Analysis of the Enzymes Involved in Haloarchaeal Denitrification. Bernabeu E, Miralles-Robledillo JM, Giani M, Valdés E, Martínez-Espinosa RM, Pire C. Biomolecules 11 1043 (2021)


Reviews citing this publication (6)

  1. (Per)chlorate in Biology on Earth and Beyond. Youngblut MD, Wang O, Barnum TP, Coates JD. Annu Rev Microbiol 70 435-457 (2016)
  2. Biotechnological Applications of Microbial (Per)chlorate Reduction. Wang O, Coates JD. Microorganisms 5 E76 (2017)
  3. Microbial Synthesis and Transformation of Inorganic and Organic Chlorine Compounds. Atashgahi S, Liebensteiner MG, Janssen DB, Smidt H, Stams AJM, Sipkema D. Front Microbiol 9 3079 (2018)
  4. Advancing Our Understanding of Pyranopterin-Dithiolene Contributions to Moco Enzyme Catalysis. Burgmayer SJN, Kirk ML. Molecules 28 7456 (2023)
  5. Integration of molecular and computational approaches paints a holistic portrait of obscure metabolisms. Reyes-Umana V, Ewens SD, Meier DAO, Coates JD. mBio e0043123 (2023)
  6. Making Moco: A Personal History. Burgmayer SJN. Molecules 28 7296 (2023)

Articles citing this publication (18)

  1. A bioinspired iron catalyst for nitrate and perchlorate reduction. Ford CL, Park YJ, Matson EM, Gordon Z, Fout AR. Science 354 741-743 (2016)
  2. Genome-resolved metagenomics identifies genetic mobility, metabolic interactions, and unexpected diversity in perchlorate-reducing communities. Barnum TP, Figueroa IA, Carlström CI, Lucas LN, Engelbrektson AL, Coates JD. ISME J 12 1568-1581 (2018)
  3. Structural and mechanistic analysis of the arsenate respiratory reductase provides insight into environmental arsenic transformations. Glasser NR, Oyala PH, Osborne TH, Santini JM, Newman DK. Proc Natl Acad Sci U S A 115 E8614-E8623 (2018)
  4. Mechanism of H2S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism Azospira suillum PS. Mehta-Kolte MG, Loutey D, Wang O, Youngblut MD, Hubbard CG, Wetmore KM, Conrad ME, Coates JD. mBio 8 e02023-16 (2017)
  5. Integrating single-cobalt-site and electric field of boron nitride in dechlorination electrocatalysts by bioinspired design. Min Y, Zhou X, Chen JJ, Chen W, Zhou F, Wang Z, Yang J, Xiong C, Wang Y, Li F, Yu HQ, Wu Y. Nat Commun 12 303 (2021)
  6. Curated BLAST for Genomes. Price MN, Arkin AP. mSystems 4 e00072-19 (2019)
  7. Mechanism Across Scales: A Holistic Modeling Framework Integrating Laboratory and Field Studies for Microbial Ecology. Lui LM, Majumder EL, Smith HJ, Carlson HK, von Netzer F, Fields MW, Stahl DA, Zhou J, Hazen TC, Baliga NS, Adams PD, Arkin AP. Front Microbiol 12 642422 (2021)
  8. Genetic and phylogenetic analysis of dissimilatory iodate-reducing bacteria identifies potential niches across the world's oceans. Reyes-Umana V, Henning Z, Lee K, Barnum TP, Coates JD. ISME J 16 38-49 (2022)
  9. Implications of Pyran Cyclization and Pterin Conformation on Oxidized Forms of the Molybdenum Cofactor. Gisewhite DR, Yang J, Williams BR, Esmail A, Stein B, Kirk ML, Burgmayer SJN. J Am Chem Soc 140 12808-12818 (2018)
  10. Reaction mechanism of sterol hydroxylation by steroid C25 dehydrogenase - Homology model, reactivity and isoenzymatic diversity. Rugor A, Wójcik-Augustyn A, Niedzialkowska E, Mordalski S, Staroń J, Bojarski A, Szaleniec M. J Inorg Biochem 173 28-43 (2017)
  11. Evidence for Biotic Perchlorate Reduction in Naturally Perchlorate-Rich Sediments of Pilot Valley Basin, Utah. Lynch KL, Jackson WA, Rey K, Spear JR, Rosenzweig F, Munakata-Marr J. Astrobiology 19 629-641 (2019)
  12. Functional Redundancy in Perchlorate and Nitrate Electron Transport Chains and Rewiring Respiratory Pathways to Alter Terminal Electron Acceptor Preference. Wang O, Melnyk RA, Mehta-Kolte MG, Youngblut MD, Carlson HK, Coates JD. Front Microbiol 9 376 (2018)
  13. Oxygen Generation via Water Splitting by a Novel Biogenic Metal Ion-Binding Compound. Dershwitz P, Bandow NL, Yang J, Semrau JD, McEllistrem MT, Heinze RA, Fonseca M, Ledesma JC, Jennett JR, DiSpirito AM, Athwal NS, Hargrove MS, Bobik TA, Zischka H, DiSpirito AA. Appl Environ Microbiol 87 e0028621 (2021)
  14. How does Mo-dependent perchlorate reductase work in the decomposition of oxyanions? Sun SQ, Chen SL. Dalton Trans 48 5683-5691 (2019)
  15. Identification of a parasitic symbiosis between respiratory metabolisms in the biogeochemical chlorine cycle. Barnum TP, Cheng Y, Hill KA, Lucas LN, Carlson HK, Coates JD. ISME J 14 1194-1206 (2020)
  16. Transcriptional response to prolonged perchlorate exposure in the methanogen Methanosarcina barkeri and implications for Martian habitability. Harris RL, Schuerger AC, Wang W, Tamama Y, Garvin ZK, Onstott TC. Sci Rep 11 12336 (2021)
  17. Characterisation of the redox centers of ethylbenzene dehydrogenase. Hagel C, Blaum B, Friedrich T, Heider J. J Biol Inorg Chem 27 143-154 (2022)
  18. Chlorine redox chemistry is widespread in microbiology. Barnum TP, Coates JD. ISME J 17 70-83 (2023)


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