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Annual Review of Biochemistry

Volume 91, 2022

Emerging Chemical Diversity and Potential Applications of Enzymes in the DMSO Reductase Superfamily

Abstract

Molybdenum- and tungsten-dependent proteins catalyze essential processes in living organisms and biogeochemical cycles. Among these enzymes, members of the dimethyl sulfoxide (DMSO) reductase superfamily are considered the most diverse, facilitating a wide range of chemical transformations that can be categorized as oxygen atom installation, removal, and transfer. Importantly, DMSO reductase enzymes provide high efficiency and excellent selectivity while operating under mild conditions without conventional oxidants such as oxygen or peroxides. Despite the potential utility of these enzymes as biocatalysts, such applications have not been fully explored. In addition, the vast majority of DMSO reductase enzymes still remain uncharacterized. In this review, we describe the reactivities, proposed mechanisms, and potential synthetic applications of selected enzymes in the DMSO reductase superfamily. We also highlight emerging opportunities to discover new chemical activity and current challenges in studying and engineering proteins in the DMSO reductase superfamily.

Keyword(s): biocatalysis, DMSO reductase, molybdopterins, tungstopterins
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/content/journals/10.1146/annurev-biochem-032620-110804
2022-06-21
2024-04-19
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Literature Cited

  1. 1.
    Mitchell PCH, Outteridge T, Kloska K, McMahon S, Epshteyn Y et al. 2020. Molybdenum and molybdenum compounds. Ullmann's Encycl. Ind. Chem. https://doi.org/10.1002/14356007.a16_655.pub2
    [Crossref] [Google Scholar]
  2. 2.
    Fürstner A. 2013. Alkyne metathesis on the rise. Angew. Chem. Int. Ed. 52:102794–819
     [Google Scholar]
  3. 3.
    Schrock RR. 2004. Recent advances in olefin metathesis by molybdenum and tungsten imido alkylidene complexes. J. Mol. Catal. A Chem. 213:121–30
     [Google Scholar]
  4. 4.
    Shen Y, Jiang P, Wai PT, Gu Q, Zhang W. 2019. Recent progress in application of molybdenum-based catalysts for epoxidation of alkenes. Catalysts 9:131
     [Google Scholar]
  5. 5.
    Tzirakis MD, Lykakis IN, Orfanopoulos M. 2009. Decatungstate as an efficient photocatalyst in organic chemistry. Chem. Soc. Rev. 38:92609–21
     [Google Scholar]
  6. 6.
    Belda O, Moberg C. 2004. Molybdenum-catalyzed asymmetric allylic alkylations. Acc. Chem. Res. 37:3159–67
     [Google Scholar]
  7. 7.
    Maia LB, Moura I, Moura JJG 2017. Molybdenum and tungsten-containing enzymes: an overview. Molybdenum and Tungsten Enzymes: Biochemistry R Hille, C Schulzke, ML Kirk 1–80 Cambridge, UK: R. Soc. Chem.
     [Google Scholar]
  8. 8.
    Tanabe Y, Nishibayashi Y. 2021. Comprehensive insights into synthetic nitrogen fixation assisted by molecular catalysts under ambient or mild conditions. Chem. Soc. Rev. 50:85201–42
     [Google Scholar]
  9. 9.
    Seefeldt LC, Yang Z-Y, Lukoyanov DA, Harris DF, Dean DR et al. 2020. Reduction of substrates by nitrogenases. Chem. Rev. 120:125082–106
     [Google Scholar]
  10. 10.
    Gladyshev VN, Zhang Y 2017. Abundance, ubiquity and evolution of molybdoenzymes. Molybdenum and Tungsten Enzymes: Biochemistry R Hille, C Schulzke, ML Kirk 81–99 Cambridge, UK: R. Soc. Chem.
     [Google Scholar]
  11. 11.
    Seelmann CS, Willistein M, Heider J, Boll M. 2020. Tungstoenzymes: occurrence, catalytic diversity and cofactor synthesis. Inorganics 8:844
     [Google Scholar]
  12. 12.
    Hille R, Hall J, Basu P. 2014. The mononuclear molybdenum enzymes. Chem. Rev. 114:73963–4038
     [Google Scholar]
  13. 13.
    Miralles-Robledillo JM, Torregrosa-Crespo J, Martínez-Espinosa RM, Pire C. 2019. DMSO reductase family: phylogenetics and applications of extremophiles. Int. J. Mol. Sci. 20:133349
     [Google Scholar]
  14. 14.
    Kirk ML, Stein B 2013. Molybdenum enzymes. Comprehensive Inorganic Chemistry II J Reedijk, K Poeppelmeier 263–93 Amsterdam: Elsevier. , 2nd ed..
     [Google Scholar]
  15. 15.
    Rothery RA, Stein B, Solomonson M, Kirk ML, Weiner JH. 2012. Pyranopterin conformation defines the function of molybdenum and tungsten enzymes. PNAS 109:3714773–78
     [Google Scholar]
  16. 16.
    Chan MK, Mukund S, Kletzin A, Adams MW, Rees DC. 1995. Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase. Science 267:52031463–69
     [Google Scholar]
  17. 17.
    Rothery RA, Workun GJ, Weiner JH. 2008. The prokaryotic complex iron–sulfur molybdoenzyme family. Biochim. Biophys. Acta Biomembr. 1778:91897–929
     [Google Scholar]
  18. 18.
    Magalon A, Fedor JG, Walburger A, Weiner JH. 2011. Molybdenum enzymes in bacteria and their maturation. Coord. Chem. Rev. 255:91159–78
     [Google Scholar]
  19. 19.
    Hong B, Luo T, Lei X. 2020. Late-stage diversification of natural products. ACS Cent. Sci. 6:5622–35
     [Google Scholar]
  20. 20.
    White MC, Zhao J. 2018. Aliphatic C–H oxidations for late-stage functionalization. J. Am. Chem. Soc. 140:4313988–89
     [Google Scholar]
  21. 21.
    Fessner ND. 2019. P450 monooxygenases enable rapid late-stage diversification of natural products via C–H bond activation. ChemCatChem 11:92226–42
     [Google Scholar]
  22. 22.
    Wohlgemuth R 2013. Development of sustainable biocatalytic reduction processes for organic chemists. Synthetic Methods for Biologically Active Molecules E Brenna 1–25 Weinheim, Ger: Wiley-VCH
     [Google Scholar]
  23. 23.
    Distefano V, Borgstedt HH. 1964. Reduction of dimethylsulfoxide to dimethylsulfide in the cat. Science 144:36221137–38
     [Google Scholar]
  24. 24.
    Tiews J, Scharrer E, Harre N, Flögel L, Jöchle W. 1975. Metabolism and excretion of dimethyl sulfoxide in cows and calves after topical and parenteral application. Ann. N. Y. Acad. Sci. 243:1139–50
     [Google Scholar]
  25. 25.
    Zinder SH, Brock TD. 1978. Dimethyl sulphoxide reduction by micro-organisms. Microbiology 105:2335–42
     [Google Scholar]
  26. 26.
    Zinder SH, Brock TD. 1978. Dimethyl sulfoxide as an electron acceptor for anaerobic growth. Arch. Microbiol. 116:135–40
     [Google Scholar]
  27. 27.
    Simala-Grant JL, Weiner JH 1998. Modulation of the substrate specificity of Escherichia coli dimethylsulfoxide reductase. Eur. J. Biochem. 251:1510–15
     [Google Scholar]
  28. 28.
    Weiner JH, Shaw G, Turner RJ, Trieber CA. 1993. The topology of the anchor subunit of dimethyl sulfoxide reductase of Escherichia coli. J. Biol. Chem. 268:53238–44
     [Google Scholar]
  29. 29.
    Sambasivarao D, Scraba DG, Trieber C, Weiner JH. 1990. Organization of dimethyl sulfoxide reductase in the plasma membrane of Escherichia coli. J. Bacteriol. 172:105938–48
     [Google Scholar]
  30. 30.
    Miguel L, Meganthan R. 1991. Electron donors and the quinone involved in dimethyl sulfoxide reduction in Escherichia coli. Curr. Microbiol. 22:2109–15
     [Google Scholar]
  31. 31.
    Garton SD, Hilton J, Oku H, Crouse BR, Rajagopalan KV, Johnson MK. 1997. Active site structures and catalytic mechanism of Rhodobacter sphaeroides dimethyl sulfoxide reductase as revealed by resonance Raman spectroscopy. J. Am. Chem. Soc. 119:5212906–16
     [Google Scholar]
  32. 32.
    McAlpine AS, McEwan AG, Bailey S. 1998. The high resolution crystal structure of DMSO reductase in complex with DMSO. J. Mol. Biol. 275:4613–23
     [Google Scholar]
  33. 33.
    Cobb N, Conrads T, Hille R. 2005. Mechanistic studies of Rhodobacter sphaeroides Me2SO reductase. J. Biol. Chem. 280:1211007–17
     [Google Scholar]
  34. 34.
    Bennett B, Benson N, McEwan AG, Bray RC. 1994. Multiple states of the molybdenum centre of dimethylsulphoxide reductase from Rhodobacter capsulatus revealed by EPR spectroscopy. Eur. J. Biochem. 225:1321–31
     [Google Scholar]
  35. 35.
    Mtei RP, Lyashenko G, Stein B, Rubie N, Hille R, Kirk ML 2011. Spectroscopic and electronic structure studies of a dimethyl sulfoxide reductase catalytic intermediate: implications for electron- and atom-transfer reactivity. J. Am. Chem. Soc. 133:259762–74
     [Google Scholar]
  36. 36.
    Tenderholt AL, Hodgson KO, Hedman B, Holm RH, Solomon EI. 2012. Substrate and metal control of barrier heights for oxo transfer to Mo and W bis-dithiolene sites. Inorg. Chem. 51:63436–42
     [Google Scholar]
  37. 37.
    Simala-Grant JL, Weiner JH 1996. Kinetic analysis and substrate specificity of Escherichia coli dimethyl sulfoxide reductase. Microbiology 142:113231–39
     [Google Scholar]
  38. 38.
    Nosek V, Míšek J. 2019. Enzymatic kinetic resolution of chiral sulfoxides – an enantiocomplementary approach. Chem. Commun. 55:7010480–83
     [Google Scholar]
  39. 39.
    Dos Santos J-P, Iobbi-Nivol C, Couillault C, Giordano G, Méjean V 1998. Molecular analysis of the trimethylamine N-oxide (TMAO) reductase respiratory system from a Shewanella species. J. Mol. Biol. 284:2421–33
     [Google Scholar]
  40. 40.
    Struwe MA, Kalimuthu P, Luo Z, Zhong Q, Ellis D et al. 2021. Active site architecture reveals coordination sphere flexibility and specificity determinants in a group of closely related molybdoenzymes. J. Biol. Chem. 296:100672
     [Google Scholar]
  41. 41.
    Johnson KE, Rajagopalan KV. 2001. An active site tyrosine influences the ability of the dimethyl sulfoxide reductase family of molybdopterin enzymes to reduce S-oxides. J. Biol. Chem. 276:1613178–85
     [Google Scholar]
  42. 42.
    Pollock VV, Barber MJ. 2001. Kinetic and mechanistic properties of biotin sulfoxide reductase. Biochemistry 40:51430–40
     [Google Scholar]
  43. 43.
    Del Campillo-Campbell A, Campbell A. 1982. Molybdenum cofactor requirement for biotin sulfoxide reduction in Escherichia coli. J. Bacteriol. 149:2469–78
     [Google Scholar]
  44. 44.
    Makukhin N, Havelka V, Poláchová E, Rampírová P, Tarallo V et al. 2019. Resolving oxidative damage to methionine by an unexpected membrane-associated stereoselective reductase discovered using chiral fluorescent probes. FEBS J 286:204024–35
     [Google Scholar]
  45. 45.
    Hanlon SP, Graham DL, Hogan PJ, Holt RA, Reeve CD et al. 1998. Asymmetric reduction of racemic sulfoxides by dimethyl sulfoxide reductases from Rhodobacter capsulatus, Escherichia coli and Proteus species. Microbiology 144:82247–53
     [Google Scholar]
  46. 46.
    Tarrago L, Grosse S, Lemaire D, Faure L, Tribout M et al. 2020. Reduction of protein bound methionine sulfoxide by a periplasmic dimethyl sulfoxide reductase. Antioxidants 9:7616
     [Google Scholar]
  47. 47.
    Abo M, Dejima M, Asano F, Okubo A, Yamazaki S. 2000. Electrochemical enzymatic deoxygenation of chiral sulfoxides utilizing DMSO reductase. Tetrahedron: Asymmetry 11:3823–28
     [Google Scholar]
  48. 48.
    Fernández I, Khiar N. 2003. Recent developments in the synthesis and utilization of chiral sulfoxides. Chem. Rev. 103:93651–706
     [Google Scholar]
  49. 49.
    Bentley R. 2005. Role of sulfur chirality in the chemical processes of biology. Chem. Soc. Rev. 34:7609–24
     [Google Scholar]
  50. 50.
    Han J, Soloshonok VA, Klika KD, Drabowicz J, Wzorek A. 2018. Chiral sulfoxides: advances in asymmetric synthesis and problems with the accurate determination of the stereochemical outcome. Chem. Soc. Rev. 47:41307–50
     [Google Scholar]
  51. 51.
    Wojaczyńska E, Wojaczyński J. 2020. Modern stereoselective synthesis of chiral sulfinyl compounds. Chem. Rev. 120:104578–611
     [Google Scholar]
  52. 52.
    Garzón-Posse F, Becerra-Figueroa L, Hernández-Arias J, Gamba-Sánchez D. 2018. Whole cells as biocatalysts in organic transformations. Molecules 23:61265
     [Google Scholar]
  53. 53.
    Wang J, Frings M, Bolm C. 2014. Iron-catalyzed imidative kinetic resolution of racemic sulfoxides. Chem. Eur. J. 20:4966–69
     [Google Scholar]
  54. 54.
    Komatsu N, Hashizume M, Sugita T, Uemura S. 1993. Kinetic resolution of sulfoxides catalyzed by chiral titanium–binaphthol complex. J. Org. Chem. 58:267624–26
     [Google Scholar]
  55. 55.
    Anselmi S, Aggarwal N, Moody TS, Castagnolo D. 2021. Unconventional biocatalytic approaches to the synthesis of chiral sulfoxides. ChemBioChem 22:2298–307
     [Google Scholar]
  56. 56.
    Luckarift HR, Dalton H, Sharma ND, Boyd DR, Holt RA. 2004. Isolation and characterisation of bacterial strains containing enantioselective DMSO reductase activity: application to the kinetic resolution of racemic sulfoxides. Appl. Microbiol. Biotechnol. 65:6678–85
     [Google Scholar]
  57. 57.
    Scheline RR, Williams RT, Wit JG. 1960. Biological dehydroxylation. Nature 188:4753849–50
     [Google Scholar]
  58. 58.
    Maini Rekdal V, Nol Bernadino P, Luescher MU, Kiamehr S, Le C et al. 2020. A widely distributed metalloenzyme class enables gut microbial metabolism of host- and diet-derived catechols. eLife 9:e50845
     [Google Scholar]
  59. 59.
    McGivern BB, Tfaily MM, Borton MA, Kosina SM, Daly RA et al. 2021. Decrypting bacterial polyphenol metabolism in an anoxic wetland soil. Nat. Commun. 12:12466
     [Google Scholar]
  60. 60.
    Sweeny DJ, Li WQ, Clough J, Bhamidipati S, Singh R et al. 2010. Metabolism of fostamatinib, the oral methylene phosphate prodrug of the spleen tyrosine kinase inhibitor R406 in humans: contribution of hepatic and gut bacterial processes to the overall biotransformation. Drug Metab. Dispos. 38:71166–76
     [Google Scholar]
  61. 61.
    Peppercorn MA, Goldman P. 1972. Caffeic acid metabolism by gnotobiotic rats and their intestinal bacteria. PNAS 69:61413–15
     [Google Scholar]
  62. 62.
    Maini Rekdal V, Bess EN, Bisanz JE, Turnbaugh PJ, Balskus EP. 2019. Discovery and inhibition of an interspecies gut bacterial pathway for Levodopa metabolism. Science 364:6445eaau6323
     [Google Scholar]
  63. 63.
    Hansen CA, Frost JW. 2002. Deoxygenation of polyhydroxybenzenes: an alternative strategy for the benzene-free synthesis of aromatic chemicals. J. Am. Chem. Soc. 124:215926–27
     [Google Scholar]
  64. 64.
    Yu P, Xie X, Tan P, Zhang W, Wang Z et al. 2020. Catalytic cleavage of the C–O bond in 2,6-dimethoxyphenol without external hydrogen or organic solvent using catalytic vanadium metal. Front. Chem. 8:636
     [Google Scholar]
  65. 65.
    Natte K, Narani A, Goyal V, Sarki N, Jagadeesh RV. 2020. Synthesis of functional chemicals from lignin-derived monomers by selective organic transformations. Adv. Synth. Catal. 362:235143–69
     [Google Scholar]
  66. 66.
    Mäki-Arvela P, Murzin DY. 2017. Hydrodeoxygenation of lignin-derived phenols: from fundamental studies towards industrial applications. Catalysts 7:9265
     [Google Scholar]
  67. 67.
    Spormann AM, Widdel F. 2000. Metabolism of alkylbenzenes, alkanes, and other hydrocarbons in anaerobic bacteria. Biodegradation 11:285–105
     [Google Scholar]
  68. 68.
    Ji Y, Mao G, Wang Y, Bartlam M. 2013. Structural insights into diversity and n-alkane biodegradation mechanisms of alkane hydroxylases. Front. Microbiol. 4:58
     [Google Scholar]
  69. 69.
    So CM, Phelps CD, Young LY. 2003. Anaerobic transformation of alkanes to fatty acids by a sulfate-reducing bacterium, strain Hxd3. Appl. Environ. Microbiol. 69:73892–900
     [Google Scholar]
  70. 70.
    Kniemeyer O, Musat F, Sievert SM, Knittel K, Wilkes H et al. 2007. Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449:7164898–901
     [Google Scholar]
  71. 71.
    Ball HA, Johnson HA, Reinhard M, Spormann AM 1996. Initial reactions in anaerobic ethylbenzene oxidation by a denitrifying bacterium, strain EB1. J. Bacteriol. 178:195755–61
     [Google Scholar]
  72. 72.
    Kniemeyer O, Heider J. 2001. Ethylbenzene dehydrogenase, a novel hydrocarbon-oxidizing molybdenum/iron-sulfur/heme enzyme. J. Biol. Chem. 276:2421381–86
     [Google Scholar]
  73. 73.
    Kloer DP, Hagel C, Heider J, Schulz GE. 2006. Crystal structure of ethylbenzene dehydrogenase from Aromatoleum aromaticum. Structure 14:91377–88
     [Google Scholar]
  74. 74.
    Cunane LM, Chen Z-W, Shamala N, Mathews FS, Cronin CN, McIntire WS. 2000. Structures of the flavocytochrome p-cresol methylhydroxylase and its enzyme-substrate complex: Gated substrate entry and proton relays support the proposed catalytic mechanism. J. Mol. Biol. 295:2357–74
     [Google Scholar]
  75. 75.
    Szaleniec M, Hagel C, Menke M, Nowak P, Witko M, Heider J. 2007. Kinetics and mechanism of oxygen-independent hydrocarbon hydroxylation by ethylbenzene dehydrogenase. Biochemistry 46:257637–46
     [Google Scholar]
  76. 76.
    Szaleniec M, Witko M, Heider J. 2008. Quantum chemical modelling of the C–H cleavage mechanism in oxidation of ethylbenzene and its derivates by ethylbenzene dehydrogenase. J. Mol. Catal. A Chem. 286:1128–36
     [Google Scholar]
  77. 77.
    Szaleniec M, Borowski T, Schühle K, Witko M, Heider J. 2010. Ab inito modeling of ethylbenzene dehydrogenase reaction mechanism. J. Am. Chem. Soc. 132:176014–24
     [Google Scholar]
  78. 78.
    Huang X, Groves JT. 2017. Beyond ferryl-mediated hydroxylation: 40 years of the rebound mechanism and C–H activation. J. Biol. Inorg. Chem. 22:2185–207
     [Google Scholar]
  79. 79.
    Szaleniec M, Dudzik A, Kozik B, Borowski T, Heider J, Witko M. 2014. Mechanistic basis for the enantioselectivity of the anaerobic hydroxylation of alkylaromatic compounds by ethylbenzene dehydrogenase. J. Inorg. Biochem. 139:9–20
     [Google Scholar]
  80. 80.
    Johnson HA, Pelletier DA, Spormann AM. 2001. Isolation and characterization of anaerobic ethylbenzene dehydrogenase, a novel Mo-Fe-S enzyme. J. Bacteriol. 183:154536–42
     [Google Scholar]
  81. 81.
    Knack D, Hagel C, Szaleniec M, Dudzik A, Salwinski A, Heider J. 2012. Substrate and inhibitor spectra of ethylbenzene dehydrogenase: perspectives on application potential and catalytic mechanism. Appl. Environ. Microbiol. 78:186475–82
     [Google Scholar]
  82. 82.
    Dudzik A, Kozik B, Tataruch M, Wójcik A, Knack D et al. 2013. The reaction mechanism of chiral hydroxylation of p-OH and p-NH2 substituted compounds by ethylbenzene dehydrogenase. Can. J. Chem. 91:9775–86
     [Google Scholar]
  83. 83.
    Tataruch M, Heider J, Bryjak J, Nowak P, Knack D et al. 2014. Suitability of the hydrocarbon-hydroxylating molybdenum-enzyme ethylbenzene dehydrogenase for industrial chiral alcohol production. J. Biotechnol. 192:400–9
     [Google Scholar]
  84. 84.
    Strijkstra A, Trautwein K, Jarling R, Wöhlbrand L, Dörries M et al. 2014. Anaerobic activation of p-cymene in denitrifying betaproteobacteria: methyl group hydroxylation versus addition to fumarate. Appl. Environ. Microbiol. 80:247592–603
     [Google Scholar]
  85. 85.
    Szaleniec M, Wojtkiewicz AM, Bernhardt R, Borowski T, Donova M. 2018. Bacterial steroid hydroxylases: enzyme classes, their functions and comparison of their catalytic mechanisms. Appl. Microbiol. Biotechnol. 102:198153–71
     [Google Scholar]
  86. 86.
    Rugor A, Wójcik-Augustyn A, Niedzialkowska E, Mordalski S, Staroń J et al. 2017. Reaction mechanism of sterol hydroxylation by steroid C25 dehydrogenase – homology model, reactivity and isoenzymatic diversity. J. Inorg. Biochem. 173:28–43
     [Google Scholar]
  87. 87.
    Jacoby C, Eipper J, Warnke M, Tiedt O, Mergelsberg M et al. 2018. Four molybdenum-dependent steroid C-25 hydroxylases: heterologous overproduction, role in steroid degradation, and application for 25-hydroxyvitamin D3 synthesis. mBio 9:3e00694–18
     [Google Scholar]
  88. 88.
    Jacoby C, Ferlaino S, Bezold D, Jessen H, Müller M, Boll M. 2020. ATP-dependent hydroxylation of an unactivated primary carbon with water. Nat. Commun. 11:13906
     [Google Scholar]
  89. 89.
    Rugor A, Tataruch M, Staroń J, Dudzik A, Niedzialkowska E et al. 2017. Regioselective hydroxylation of cholecalciferol, cholesterol and other sterol derivatives by steroid C25 dehydrogenase. Appl. Microbiol. Biotechnol. 101:31163–74
     [Google Scholar]
  90. 90.
    Heider J, Schühle K 2013. Anaerobic biodegradation of hydrocarbons including methane. The Prokaryotes E Rosenberg, EF DeLong, S Lory, E Stackebrandt, F Thompson 605–34 Berlin: Springer. , 4th ed..
     [Google Scholar]
  91. 91.
    Shou L-B, Liu Y-F, Zhou J, Liu Z-L, Zhou L et al. 2021. New evidence for a hydroxylation pathway for anaerobic alkane degradation supported by analyses of functional genes and signature metabolites in oil reservoirs. AMB Expr 11:118
     [Google Scholar]
  92. 92.
    Tzouras NV, Stamatopoulos IK, Papastavrou AT, Liori AA, Vougioukalakis GC. 2017. Sustainable metal catalysis in CH activation. Coord. Chem. Rev. 343:25–138
     [Google Scholar]
  93. 93.
    Abrams DJ, Provencher PA, Sorensen EJ. 2018. Recent applications of C–H functionalization in complex natural product synthesis. Chem. Soc. Rev. 47:238925–67
     [Google Scholar]
  94. 94.
    Vicens L, Olivo G, Costas M. 2020. Rational design of bioinspired catalysts for selective oxidations. ACS Catal 10:158611–31
     [Google Scholar]
  95. 95.
    Lewis JC, Coelho PS, Arnold FH. 2011. Enzymatic functionalization of carbon–hydrogen bonds. Chem. Soc. Rev. 40:42003–21
     [Google Scholar]
  96. 96.
    Kawamata Y, Yan M, Liu Z, Bao D-H, Chen J et al. 2017. Scalable, electrochemical oxidation of unactivated C–H bonds. J. Am. Chem. Soc. 139:227448–51
     [Google Scholar]
  97. 97.
    Dong J, Fernández-Fueyo E, Hollmann F, Paul CE, Pesic M et al. 2018. Biocatalytic oxidation reactions: a chemist's perspective. Angew. Chem. Int. Ed. 57:309238–61
     [Google Scholar]
  98. 98.
    Chakrabarty S, Wang Y, Perkins JC, Narayan ARH. 2020. Scalable biocatalytic C–H oxyfunctionalization reactions. Chem. Soc. Rev. 49:228137–55
     [Google Scholar]
  99. 99.
    Taylor AE, Taylor K, Tennigkeit B, Palatinszky M, Stieglmeier M et al. 2015. Inhibitory effects of C2 to C10 1-alkynes on ammonia oxidation in two Nitrososphaera species. Appl. Environ. Microbiol. 81:61942–48
     [Google Scholar]
  100. 100.
    Hyman MR, Arp DJ. 1988. Acetylene inhibition of metalloenzymes. Anal. Biochem. 173:2207–20
     [Google Scholar]
  101. 101.
    Akob DM, Sutton JM, Fierst JL, Haase KB, Baesman S et al. 2018. Acetylenotrophy: a hidden but ubiquitous microbial metabolism?. FEMS Microbiol. Ecol. 94:8fiy103
     [Google Scholar]
  102. 102.
    Schink B. 1985. Fermentation of acetylene by an obligate anaerobe, Pelobacter acetylenicus sp. nov. Arch. Microbiol. 142:3295–301
     [Google Scholar]
  103. 103.
    Kroneck PMH. 2016. Acetylene hydratase: a non-redox enzyme with tungsten and iron-sulfur centers at the active site. J. Biol. Inorg. Chem. 21:129–38
     [Google Scholar]
  104. 104.
    Rosner BM, Rainey FA, Kroppenstedt RM, Schink B. 1997. Acetylene degradation by new isolates of aerobic bacteria and comparison of acetylene hydratase enzymes. FEMS Microbiol. Lett. 148:2175–80
     [Google Scholar]
  105. 105.
    Seiffert GB, Ullmann GM, Messerschmidt A, Schink B, Kroneck PMH, Einsle O. 2007. Structure of the non-redox-active tungsten/[4Fe:4S] enzyme acetylene hydratase. PNAS 104:93073–77
     [Google Scholar]
  106. 106.
    Meckenstock RU, Krieger R, Ensign S, Kroneck PMH, Schink B. 1999. Acetylene hydratase of Pelobacter acetylenicus. Eur. J. Biochem. 264:1176–82
     [Google Scholar]
  107. 107.
    Vincent MA, Hillier IH, Periyasamy G, Burton NA. 2010. A DFT study of the possible role of vinylidene and carbene intermediates in the mechanism of the enzyme acetylene hydratase. Dalt. Trans. 39:163816–22
     [Google Scholar]
  108. 108.
    Antony S, Bayse CA. 2009. Theoretical studies of models of the active site of the tungstoenzyme acetylene hydratase. Organometallics 28:174938–44
     [Google Scholar]
  109. 109.
    Liao R-Z, Yu J-G, Himo F 2010. Mechanism of tungsten-dependent acetylene hydratase from quantum chemical calculations. PNAS 107:5222523–27
     [Google Scholar]
  110. 110.
    tenBrink F, Schink B, Kroneck PMH. 2011. Exploring the active site of the tungsten, iron-sulfur enzyme acetylene hydratase. J. Bacteriol. 193:51229–36
     [Google Scholar]
  111. 111.
    Habib U, Riaz M, Hofmann M. 2021. Unraveling the way acetaldehyde is formed from acetylene: a study based on DFT. ACS Omega 6:106924–33
     [Google Scholar]
  112. 112.
    Liao R-Z, Himo F. 2011. Theoretical study of the chemoselectivity of tungsten-dependent acetylene hydratase. ACS Catal 1:8937–44
     [Google Scholar]
  113. 113.
    Alabugin IV, Gonzalez-Rodriguez E, Kawade RK, Stepanov AA, Vasilevsky SF. 2019. Alkynes as synthetic equivalents of ketones and aldehydes: a hidden entry into carbonyl chemistry. Molecules 24:61036
     [Google Scholar]
  114. 114.
    Goodwin JA, Aponick A. 2015. Regioselectivity in the Au-catalyzed hydration and hydroalkoxylation of alkynes. Chem. Commun. 51:428730–41
     [Google Scholar]
  115. 115.
    Salvio R, Bassetti M. 2021. Sustainable hydration of alkynes promoted by first row transition metal complexes. Background, highlights and perspectives. Inorganica Chim. Acta 522:120288
     [Google Scholar]
  116. 116.
    Corma A, Leyva-Pérez A, Sabater MJ. 2011. Gold-catalyzed carbon−heteroatom bond-forming reactions. Chem. Rev. 111:31657–712
     [Google Scholar]
  117. 117.
    Hintermann L, Labonne A. 2007. Catalytic hydration of alkynes and its application in synthesis. Synthesis 2007.081121–50
     [Google Scholar]
  118. 118.
    Demming RM, Hammer SC, Nestl BM, Gergel S, Fademrecht S et al. 2019. Asymmetric enzymatic hydration of unactivated, aliphatic alkenes. Angew. Chem. Int. Ed. 58:1173–77
     [Google Scholar]
  119. 119.
    Alipui OD, Zhang D, Schulz H. 2002. Direct hydration of 3-octynoyl-CoA by crotonase: a missing link in Konrad Bloch's enzymatic studies with 3-alkynoyl thioesters. Biochem. Biophys. Res. Commun. 292:51171–74
     [Google Scholar]
  120. 120.
    Gushgari-Doyle S, Oremland RS, Keren R, Baesman SM, Akob DM et al. 2021. Acetylene-fueled trichloroethene reductive dechlorination in a groundwater enrichment culture. mBio 12:1e02724–20
     [Google Scholar]
  121. 121.
    Brune A, Schink B. 1990. Pyrogallol-to-phloroglucinol conversion and other hydroxyl-transfer reactions catalyzed by cell extracts of Pelobacter acidigallici. J. Bacteriol. 172:21070–76
     [Google Scholar]
  122. 122.
    Reichenbecher W, Brune A, Schink B. 1994. Transhydroxylase of Pelobacter acidigallici: a molybdoenzyme catalyzing the conversion of pyrogallol to phloroglucinol. Biochim. Biophys. Acta Protein Struct. Mol. Enzymol. 1204:2217–24
     [Google Scholar]
  123. 123.
    Krumholz LR, Bryant MP. 1986. Eubacterium oxidoreducens sp. nov. requiring H2 or formate to degrade gallate, pyrogallol, phloroglucinol and quercetin. Arch. Microbiol. 144:18–14
     [Google Scholar]
  124. 124.
    Baas D, Rétey J. 1999. Cloning, sequencing and heterologous expression of pyrogallol-phloroglucinol transhydroxylase from Pelobacter acidigallici. Eur. J. Biochem. 265:3896–901
     [Google Scholar]
  125. 125.
    Messerschmidt A, Niessen H, Abt D, Einsle O, Schink B, Kroneck PM. 2004. Crystal structure of pyrogallol–phloroglucinol transhydroxylase, an Mo enzyme capable of intermolecular hydroxyl transfer between phenols. PNAS 101:3211571–76
     [Google Scholar]
  126. 126.
    Reichenbecher W, Schink B. 1999. Towards the reaction mechanism of pyrogallol–phloroglucinol transhydroxylase of Pelobacter acidigallici. Biochim. Biophys. Acta Protein Struct. Mol. Enzymol. 1430:2245–53
     [Google Scholar]
  127. 127.
    Paizs C, Bartlewski-Hof U, Rétey J. 2007. Investigation of the mechanism of action of pyrogallol–phloroglucinol transhydroxylase by using putative intermediates. Chem. Eur. J. 13:102805–11
     [Google Scholar]
  128. 128.
    Andreas B, Sylvia S, Bernhard S 1992. Sequential transhydroxylations converting hydroxyhydroquinone to phloroglucinol in the strictly anaerobic, fermentative bacterium Pelobacter massiliensis. Appl. Environ. Microbiol. 58:61861–68
     [Google Scholar]
  129. 129.
    Águeda M-F, Daniel P, Patricia M, Bodo P, Bernhard S et al. 2015. Identification of the gene cluster for the anaerobic degradation of 3,5-dihydroxybenzoate (α-resorcylate) in Thauera aromatica strain AR-1. Appl. Environ. Microbiol. 81:207201–14
     [Google Scholar]
  130. 130.
    Darley PI, Hellstern JA, Medina-Bellver JI, Marqués S, Schink B, Philipp B. 2007. Heterologous expression and identification of the genes involved in anaerobic degradation of 1,3-dihydroxybenzene (resorcinol) in Azoarcus anaerobius. J. Bacteriol. 189:103824–33
     [Google Scholar]
  131. 131.
    Liu Y, Liu S, Xiao Y 2017. Transition-metal-catalyzed synthesis of phenols and aryl thiols. Beilstein J. Org. Chem. 13:589–611
     [Google Scholar]
  132. 132.
    Panzella L, Napolitano A. 2017. Natural phenol polymers: recent advances in food and health applications. Antioxidants 6:230
     [Google Scholar]
  133. 133.
    Alonso DA, Nájera C, Pastor IM, Yus M. 2010. Transition-metal-catalyzed synthesis of hydroxylated arenes. Chem. Eur. J. 16:185274–84
     [Google Scholar]
  134. 134.
    Ullrich R, Hofrichter M. 2007. Enzymatic hydroxylation of aromatic compounds. Cell. Mol. Life Sci. 64:3271–93
     [Google Scholar]
  135. 135.
    Paul CE, Eggerichs D, Westphal AH, Tischler D, van Berkel WJH. 2021. Flavoprotein monooxygenases: versatile biocatalysts. Biotechnol. Adv. 51:107712
     [Google Scholar]
  136. 136.
    Zallot R, Oberg N, Gerlt JA. 2019. The EFI web resource for genomic enzymology tools: leveraging protein, genome, and metagenome databases to discover novel enzymes and metabolic pathways. Biochemistry 58:414169–82
     [Google Scholar]
  137. 137.
    Pedrós-Alió C, Manrubia S. 2016. The vast unknown microbial biosphere. PNAS 113:246585–87
     [Google Scholar]
  138. 138.
    Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ et al. 2004. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:697837–43
     [Google Scholar]
  139. 139.
    Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D et al. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:566766–74
     [Google Scholar]
  140. 140.
    Nayfach S, Roux S, Seshadri R, Udwary D, Varghese N et al. 2021. A genomic catalog of Earth's microbiomes. Nat. Biotechnol. 39:4499–509
     [Google Scholar]
  141. 141.
    Imlay JA. 2006. Iron-sulphur clusters and the problem with oxygen. Mol. Microbiol. 59:41073–82
     [Google Scholar]
  142. 142.
    Glasser NR, Oyala PH, Osborne TH, Santini JM, Newman DK. 2018. Structural and mechanistic analysis of the arsenate respiratory reductase provides insight into environmental arsenic transformations. PNAS 115:378614–23
     [Google Scholar]
  143. 143.
    Mintmier B, Nassif S, Stolz JF, Basu P. 2020. Functional mononuclear molybdenum enzymes: challenges and triumphs in molecular cloning, expression, and isolation. J. Biol. Inorg. Chem. 25:4547–69
     [Google Scholar]
  144. 144.
    Iobbi-Nivol C, Leimkühler S. 2013. Molybdenum enzymes, their maturation and molybdenum cofactor biosynthesis in Escherichia coli. Biochim. Biophys. Acta Bioenerg. 1827:81086–101
     [Google Scholar]
  145. 145.
    Zupok A, Iobbi-Nivol C, Méjean V, Leimkühler S. 2019. The regulation of Moco biosynthesis and molybdoenzyme gene expression by molybdenum and iron in bacteria. Metallomics 11:101602–24
     [Google Scholar]
  146. 146.
    Tang H, Rothery RA, Voss JE, Weiner JH. 2011. Correct assembly of iron-sulfur cluster FS0 into Escherichia coli dimethyl sulfoxide reductase (DmsABC) is a prerequisite for molybdenum cofactor insertion. J. Biol. Chem. 286:1715147–54
     [Google Scholar]
  147. 147.
    Neumann M, Leimkühler S. 2011. The role of system-specific molecular chaperones in the maturation of molybdoenzymes in bacteria. Biochem. Res. Int. 2011.850924
     [Google Scholar]
  148. 148.
    Ray N, Oates J, Turner RJ, Robinson C. 2003. DmsD is required for the biogenesis of DMSO reductase in Escherichia coli but not for the interaction of the DmsA signal peptide with the Tat apparatus. FEBS Lett 534:1–3156–60
     [Google Scholar]
  149. 149.
    Rabus R, Kube M, Beck A, Widdel F, Reinhardt R. 2002. Genes involved in the anaerobic degradation of ethylbenzene in a denitrifying bacterium, strain EbN1. Arch. Microbiol. 178:6506–16
     [Google Scholar]
/content/journals/10.1146/annurev-biochem-032620-110804
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Emerging Chemical Diversity and Potential Applications of Enzymes in the DMSO Reductase Superfamily
Annual Review of Biochemistry 91, 475 (2022); https://doi.org/10.1146/annurev-biochem-032620-110804
/content/journals/10.1146/annurev-biochem-032620-110804
/content/journals/10.1146/annurev-biochem-032620-110804
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