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Acetylene hydratase: a non-redox enzyme with tungsten and iron–sulfur centers at the active site

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Abstract

In living systems, tungsten is exclusively found in microbial enzymes coordinated by the pyranopterin cofactor, with additional metal coordination provided by oxygen and/or sulfur, and/or selenium atoms in diverse arrangements. Prominent examples are formate dehydrogenase, formylmethanofuran dehydrogenase, and aldehyde oxidoreductase all of which catalyze redox reactions. The bacterial enzyme acetylene hydratase (AH) stands out of its class as it catalyzes the conversion of acetylene to acetaldehyde, clearly a non-redox reaction and a reaction distinct from the reduction of acetylene to ethylene by nitrogenase. AH harbors two pyranopterins bound to W, and a [4Fe–4S] cluster. W is coordinated by four dithiolene sulfur atoms, one cysteine sulfur, and one oxygen ligand. AH activity requires a strong reductant suggesting W(IV) as the active oxidation state. Two different types of reaction pathways have been proposed. The 1.26 Å structure reveals a water molecule coordinated to W which could gain a partially positive net charge by the adjacent protonated Asp-13, enabling a direct attack of C2H2. To access the W–Asp site, a substrate channel was evolved distant from where it is found in other members of the DMSOR family. Computational studies of this second shell mechanism led to unrealistically high energy barriers, and alternative pathways were proposed where C2H2 binds directly to W. The architecture of the catalytic cavity, the specificity for C2H2 and the results from site-directed mutagenesis do not support this first shell mechanism. More investigations including structural information on the binding of C2H2 are needed to present a conclusive answer.

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References

  1. Kletzin A, Adams MWW (1996) FEMS Microbiol Rev 18:5–63. doi:10.1111/j.1574-6976.1996.tb00226.x

    Article  CAS  PubMed  Google Scholar 

  2. Hille R (2002) TIBS 27:360–367. doi:10.1016/S0968-0004(02)02107-2

    CAS  PubMed  Google Scholar 

  3. Stiefel EI (2002) Met Ions Biol Sys 39:1–29

    CAS  Google Scholar 

  4. Bevers LE, Hagedoorn P-L, Hagen WR (2009) Coord Chem Rev 253:269–290. doi:10.1016/j.ccr.2008.01.017

    Article  CAS  Google Scholar 

  5. Zhang Y, Gladyshev VN (2008) J Mol Biol 379:881–899. doi:10.1016/j.jmb.2008.03.051

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Schoepp-Cothenet B, van Lis R, Philippot P, Magalon A, Russell MJ, Nitschke W (2012) Sci Rep 2:263. doi:10.1038/srep00263

    Article  PubMed Central  PubMed  Google Scholar 

  7. Mendel RR (2013) J Biol Chem 288:13165–13172. doi:10.1074/jbc.R113.455311

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Grimaldi S, Schoepp-Cothenet B, Ceccaldi P, Guigliarelli B, Magalon A (2013) Biochim Biophys Acta 1827:1048–1085. doi:10.1016/j.bbabio.2013.01.011

    Article  CAS  PubMed  Google Scholar 

  9. Hille R, Hall J, Basu P (2014) Chem Rev 114:3963–4038. doi:10.1021/cr400443z

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Pushie MJ, Cotelesage JJ, George GN (2014) Metallomics 6:15–24. doi:10.1039/c3mt00177f

    Article  CAS  PubMed  Google Scholar 

  11. Rothery RA, Weiner JH (2015) J Biol Inorg Chem 20:349–372. doi:10.1007/s00775-014-1194-6

    Article  CAS  PubMed  Google Scholar 

  12. Maia LB, Moura JJG, Moura I (2015) J Biol Inorg Chem 20:287–309. doi:10.1007/s00775-014-1218-2

    Article  CAS  PubMed  Google Scholar 

  13. Cerqueira NMFSA, Gonzalez PJ, Fernandes PA, Moura JJG, JoaoRamos M (2015) Acc Chem Res 48:2875–2884. doi:10.1021/acs.accounts.5b00333

    Article  CAS  PubMed  Google Scholar 

  14. Leimkühler S, Iobbi-Nivol C (2015) FEMS Microbiol Rev. doi:10.1093/femsre/fuv043

    PubMed  Google Scholar 

  15. Bortels H (1936) Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene, Abteilung 2, vol 95, pp 193–218

  16. Williams RJP, Frausto da Silva JJR (2002) Biochem Biophys Res Commun 292:293–299. doi:10.1006/bbrc.2002.6518

    Article  CAS  PubMed  Google Scholar 

  17. Yamamoto I, Saiki T, Liu S-M, Ljungdahl (1983) J Biol Chem 258:1826–1832. http://www.jbc.org/content/258/3/1826

  18. Johnson MK, Rees DC, Adams MWW (1996) Chem Rev 96:2817–2839. doi:10.1021/cr950063d

    Article  CAS  PubMed  Google Scholar 

  19. Moura JJG, Brondino CD, Trincao J, Romao MJ (2004) J Biol Inorg Chem 9:791–799. doi:10.1007/s00775-004-0573-9

    Article  CAS  PubMed  Google Scholar 

  20. Andreesen JR, Makdessi K (2008) Ann NY Acad Sci 1125:215–229. doi:10.1196/annals.1419.003

    Article  CAS  PubMed  Google Scholar 

  21. Bolster MWG (1997) Pure Appl Chem 69:1251–1303

    Article  Google Scholar 

  22. Enemark JH, Cooney JJA, Wang JJ, Holm RH (2004) Chem Rev 104:1175–1200. doi:10.1021/cr020609d

    Article  CAS  PubMed  Google Scholar 

  23. Sugimoto H, Tsukube H (2008) Chem Soc Rev 37:2609–2619. doi:10.1039/b610235m

    Article  CAS  PubMed  Google Scholar 

  24. Chan MK, Mukund S, Kletzin A, Adams MWW, Rees DC (1995) Science 267:1463–1469. doi:10.1126/science.7878465

    Article  CAS  PubMed  Google Scholar 

  25. Frausto da Silva JJR, Williams RJP (2001) The biological chemistry of the elements, vol 2. Oxford University Press, Oxford

    Google Scholar 

  26. Williams RJP, Frausto da Silva JJR (2003) J Theor Biol 220:323–343. doi:10.1006/jtbi.2003.3152

    Article  CAS  PubMed  Google Scholar 

  27. Bräsen C, Esser D, Rauch B, Siebers B (2014) Microbiol Mol Biol Rev 78:89–175. doi:10.1128/MMBR.00041-13

  28. Cameron V, House CH, Brantley SL (2012) Archaea, 12 pages. doi:10.1155/2012/789278

  29. Williams RJB, Rickaby REM (2012) Evolution’s destiny: co-evolving chemistry of the environment and life. RSC Publishing. doi:10.1039/9781849735599

  30. Mann S, Thomson AJ (2015) Angew Chem Int Ed 54:7746. doi:10.1002/anie.201504131

    Article  CAS  Google Scholar 

  31. Schink B (1985) Arch Microbiol 142:295–301. doi:10.1007/BF00693407

    Article  CAS  Google Scholar 

  32. Ten Brink F (2014) Met Ions Life Sci 14:15–35. doi:10.1007/978-94-017-9269-1_2

    Article  PubMed  Google Scholar 

  33. Bu‘lock JD (1956) Quarter Rev 10:371–394. doi:10.1039/QR9561000371

    Google Scholar 

  34. Yamada EW, Jakoby WB (1958) J Biol Chem 233:706–711. http://www.jbc.org/content/233/3/706.citation

  35. Oremland RS, Voytek MA (2008) Astrobiology 8:45–58. doi:10.1089/ast.2007.0183

    Article  CAS  PubMed  Google Scholar 

  36. Abbasian F, Lockington R, Megharaj M, Naidu R (2015) Appl Biochem Biotechnol. doi:10.1007/s12010-015-1881-y

    Google Scholar 

  37. Hyman MR, Arp DJ (1988) Anal Biochem 173:207–220. doi:10.1016/0003-2697(88)90181-9

    Article  CAS  PubMed  Google Scholar 

  38. Stewart WD, Fitzgerald GP, Burris RH (1967) Proc Natl Acad Sci (USA) 58:2071–2078

    Article  CAS  Google Scholar 

  39. Burris RH (1969) Proc Roy Soc B 172:339–354. http://www.jstor.org/stable/75888

  40. Shah VK, Chisnell JR, Brill WJ (1978) Biochem Biophys Res Commun 81:232–236. doi:10.1016/0006-291X(78)91654-6

    Article  CAS  PubMed  Google Scholar 

  41. Rosner BM, Schink B (1995) J Bacteriol 177:5767–5772

    PubMed Central  CAS  PubMed  Google Scholar 

  42. Meckenstock RU, Krieger R, Ensign S, Kroneck PMH, Schink B (1999) Eur J Biochem 264:176–182. doi:10.1046/j.1432-1327.1999.00600.x

    Article  CAS  PubMed  Google Scholar 

  43. Schink B (2006) Prokaryotes 7:5–11. doi:10.1007/0-387-30747-8_1

    Article  Google Scholar 

  44. Seiffert G (2007) PhD Dissertation, University of Konstanz, Germany

  45. Ten Brink F (2010) PhD Dissertation, University of Konstanz, Germany

  46. Schmidt A, Frensch M, Schleheck D, Schink B, Müller N (2014) PLoS One 9(12):e115902. doi:10.1371/journal.pone.0115902

    Article  PubMed Central  PubMed  Google Scholar 

  47. Birch-Hirschfeld L (1932) Zentralblatt Bakteriologie und Parasitenkunde 86:113–129

    Google Scholar 

  48. Kanner D, Bartha R (1979) J Bacteriol 139:225–230

    PubMed Central  CAS  PubMed  Google Scholar 

  49. De Bont JAM, Peck MW (1980) Arch Microbiol 127:99–104. doi:10.1007/BF00428012

    Article  Google Scholar 

  50. Culbertson CW, Strohmaier FE, Oremland RS (1988) Origins Life Evol Biosph 18:397–407. doi:10.1007/BF01808218

    Article  CAS  Google Scholar 

  51. Rosner BM, Rainey FA, Kroppenstedt RM, Schink B (1997) FEMS Microbiol Lett 148:175–180. doi:10.1111/j.1574-6968.1997.tb10285.x

    Article  CAS  PubMed  Google Scholar 

  52. Miller LG, Baesman SM, Kirshtein J, Voytek MA, Oremland RS (2013) Geomicrobiol J 30:501–516. doi:10.1080/01490451.2012.732662

    Article  CAS  Google Scholar 

  53. Seiffert GB, Abt D, Ten Brink F, Fischer D, Einsle O, Kroneck PMH (2008) In: Messerschmidt A (ed) Handbook of metalloproteins, vol 4 + 5, pp 541–548. Chichester

  54. Thaddeus P (2006) Phil Trans R Soc B 361:1681–1687. doi:10.1098/rstb.2006

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  55. Kasting JF, Zahnle KJ, Walker JCG (1983) Precambrian Res 20:121–148. doi:10.1016/0301-9268(83)90069-4

    Article  CAS  Google Scholar 

  56. Zahnle KJ (1986) J Geophys Res 91:2819–2834. doi:10.1029/JD091iD02p02819

    Article  CAS  Google Scholar 

  57. Sagan C, Thompson WR (1984) Icarus 59:133–161. doi:10.1016/0019-1035(84)90018-6

    Article  CAS  Google Scholar 

  58. Schulze-Makuch D, Grinspoon DH (2005) Astrobiology 5:560–567

    Article  CAS  PubMed  Google Scholar 

  59. Cordier D, Mousis O, Lunine JI, Lavvas P, Vuitton V (2009) Astrophys J Lett 707:L128–L131. doi:10.1088/0004-637X/707/2/L128

    Article  CAS  Google Scholar 

  60. Tokano T (2009) Astrobiology 9:147–164. doi:10.1089/ast.2007.0220

    Article  CAS  PubMed  Google Scholar 

  61. Waite JH Jr, Combi MR, Ip W-H, Cravens TE, McNutt RL Jr, Kasprzak W, Yelle R, Luhmann J, Niemann H, Gell D, Magee B, Fletcher G, Lunine J, Tsen W-L (2006) Science 311:1419–1422. doi:10.1126/science.1121290

    Article  CAS  PubMed  Google Scholar 

  62. Matson DL, Castillo JC, Lunine J, Johnson TV (2007) Icarus 187:569–573. doi:10.1016/j.icarus.2006.10.016

    Article  CAS  Google Scholar 

  63. Seiffert GB, Ullmann GM, Messerschmidt A, Schink B, Kroneck PMH, Einsle O (2007) Proc Natl Acad Sci (USA) 104:3073–3077. doi:10.1073/pnas.0610407104

    Article  CAS  Google Scholar 

  64. Ten Brink F, Schink B, Kroneck PMH (2011) J Bacteriol 193:1229–1236

    Article  Google Scholar 

  65. Hille R (1996) Chem Rev 96:2757–2816. doi:10.1021/cr950061t

    Article  CAS  PubMed  Google Scholar 

  66. Stewart LJ, Bailey S, Bennett B, Charnock JM, Garner CD, McAlpine AS (2000) J Mol Biol 299:593–600. doi:10.1006/jmbi.2000.3702

  67. Abt DJ (2001) PhD Dissertation, University of Konstanz, Germany

  68. Einsle O, Niessen H, Abt DJ, Seiffert GB, Schink B, Huber R, Messerschmidt A, Kroneck PMH (2005) Acta Cryst F61:299–301. doi:10.1107/S174430910500374X

    Google Scholar 

  69. Dobbek H, Huber R (2002) Met Ions Biol Sys 39:227–26329

    CAS  Google Scholar 

  70. Burger E-M, Andrade SLA, Einsle O (2015) Curr Op Struct Biol 35:32–40. doi:10.1016/j.sbi.2015.07.016

    Article  CAS  Google Scholar 

  71. Bashford D, Karplus M (1990) Biochemistry 29:10219–11022. doi:10.1021/bi00496a010

    Article  CAS  PubMed  Google Scholar 

  72. Ullmann GM, Knapp E-W (1999) Eur Biophys J 28:533–551. doi:10.1007/s002490050236

    Article  CAS  PubMed  Google Scholar 

  73. Ullmann GM, Elisa Bombarda E (2014) In: Náray-Szabó G (ed) Protein modelling, pp 135–163. Springer, Berlin. doi:10.1007/978-3-319-09976-7_6

  74. Boll M, Einsle O, Ermler U, Kroneck PMH, Ullmann GM (2016) J Mol Microbiol Biotechnol (in press)

  75. Bas DC, Rogers DM, Jensen JH (2008) Proteins 73:765–783. doi:10.1002/prot.22102

    Article  CAS  PubMed  Google Scholar 

  76. Liao R-Z, Yu J-G, Himo F (2010) Proc Natl Acad Sci (USA) 52:22523–22527. doi:10.1073/pnas.1014060108

    Article  Google Scholar 

  77. Liu Y-F, Liao R-Z, Ding W-J, Yu J-G, Liu R-Z (2011) J Biol Inorg Chem 16:745–752. doi:10.1007/s00775-011-0775-x

    Article  CAS  PubMed  Google Scholar 

  78. Liao R-Z, Thiel W (2012) J Chem Theory Comput 8:3793–3803. doi:10.1021/ct3000684

    Article  CAS  PubMed  Google Scholar 

  79. Liao R-Z, Thiel W (2013) J Comput Chem 27:2389–2397. doi:10.1002/jcc.23403

    Google Scholar 

  80. Gilch S, Vogel M, Lorenz MW, Meyer O, Schmidt I (2009) Microbiology 155:279–284. doi:10.1099/mic.0.023721-0

    Article  CAS  PubMed  Google Scholar 

  81. Kutscheroff M Ber Bunsenges Phys Chemie 1881:1540–1542

  82. Ponomarev DA, Shevchenko SM (2007) J Chem Ed 84:1725–1726

    Article  CAS  Google Scholar 

  83. Trost BM (2002) Acc Chem Res 35:695–705. doi:10.1021/ar010068z

    Article  CAS  PubMed  Google Scholar 

  84. Hintermann L, Labonne A (2007) Synthesis 8:1121–1150. doi:10.1055/s-2007-966002

    Article  Google Scholar 

  85. Majumdar A, Sarkar S (2011) Coord Chem Rev 255:1039–1054. doi:10.1016/j.ccr.2010.11.027

    Article  CAS  Google Scholar 

  86. Das SK, Biswas D, Maiti R, Sarkar S (1996) J Am Chem Soc 118:1387–1397. doi:10.1021/ja9511580

    Article  CAS  Google Scholar 

  87. Yadav J, Das SK, Sarkar S (1997) J Am Chem Soc 119:4315–4316. doi:10.1021/ja970134l

    Article  CAS  Google Scholar 

  88. Ricard L, Weiss R, Newton WE, Chen GJ-J, McDonald JW (1978) J Am Chem Soc 100:1319–1320. doi:10.1021/ja00472a062

    Article  Google Scholar 

  89. Templeton JL, Ward BC, Chen GJ-J, McDonald JW, Newton WE (1981) Inorg Chem 20:1248–1253. doi:10.1021/ic50218a056

    Article  CAS  Google Scholar 

  90. Peschel LM, Bela FJ, Mösch-Zanetti NC (2015) Angew Chem 127:13210–13213. doi:10.1002/anie.201505764

    Article  Google Scholar 

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Acknowledgments

My thanks go to Bernhard Schink who introduced me to the subject of acetylene converting microorganisms, and to my students, coworkers and collaborators, named in the cited references, for their numerous valuable contributions. Work in the laboratory was supported by the Deutsche Forschungsgemeinschaft.

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  1. Department of Biology, University of Konstanz, Universitaetsstrasse 10, 78457, Konstanz, Germany

    Peter M. H. Kroneck

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Kroneck, P.M.H. Acetylene hydratase: a non-redox enzyme with tungsten and iron–sulfur centers at the active site. J Biol Inorg Chem 21, 29–38 (2016). https://doi.org/10.1007/s00775-015-1330-y

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