Fungal denitrification and nitric oxide reductase cytochrome P450nor

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1593, 2012, Pages 1186-1194

  Shoun, Hirofumi ^a   Fushinobu, Shinya ^a   Jiang, Li ^a   Kim, Sang Wan ^a   Wakagi, Takayoshi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Co denitrification; Denitrification by fungi; Mitochondrial anaerobic respiration; NirK; P450nor

Indexed keywords

BIODEGRADATION; CYTOCHROME; DENITRIFICATION; FUNGUS; MICROBIAL ACTIVITY; NITRIC OXIDE; PHYLOGENETICS; RESPIRATION;

BACTERIA (MICROORGANISMS); EUKARYOTA; FUNGI; PROKARYOTA;

EID: 84859074293     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0335     Document Type: Review

References (49)

1. Berks, B. C., Ferguson, S. J., Moir, J. W. & Richardson, D. J. 1995 Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. Biochim. Biophys. Acta 1232, 97-173. (doi:10.1016/0005-2728(95)00092-5)
2. Zumft, W. G. 1997 Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61, 533-616.
3. Ferguson, S. J. 1998 Nitrogen cycle enzymology. Curr. Opin. Chem. Biol. 2, 182-193. (doi:10.1016/S1367-5931(98)80059-8)
4. Shoun, H. & Tanimoto, T. 1991 Denitrification by the fungus Fusarium oxysporum and involvement of cytochrome P-450 in the respiratory nitrite reduction. J. Biol. Chem. 266, 11 078-11 082.
5. Shoun, H., Kim, D. H., Uchiyama, H. & Sugiyama, J. 1992 Denitrification by fungi. FEMS Microbiol. Lett. 73, 277-281. (doi:10.1111/j.1574-6968.1992.tb05331.x)
6. Tsuruta, S., Takaya, N., Zhang, L., Shoun, H., Kimura, K., Hamamoto, M. & Nakase, T. 1998 Denitrification by yeasts and occurrence of cytochrome P450nor in Trichosporon cutaneum. FEMS Microbiol. Lett. 168, 105-110. (doi:10.1111/j.1574-6968.1998.tb13262.x)
7. Averill, B. A. 1996 Dissimilatory nitrite and nitric oxide reductases. Chem. Rev. 96, 2951-2964. (doi:10.1021/ cr950056p)
8. Nakahara, K., Tanimoto, T., Hatano, K., Usuda, K. & Shoun, H. 1993 Cytochrome-P-450-55A1 (P-450dNIR) acts as nitric oxide reductase employing NADH as the direct electron-donor. J. Biol. Chem. 268, 8350-8355.
9. Takaya, N. & Shoun, H. 2000 Nitric oxide reduction, the last step in denitrification by Fusarium oxysporum, is obligatorily mediated by cytochrome P450nor. Mol. Gen. Genet. 263, 342-348. (doi:10.1007/s004380051177)
10. Laughlin, R. J. & Stevens, R. J. 2002 Evidence for fungal dominance of denitrification and codenitrification in a grassland soil. Soil Sci. Soc. Am. J. 66, 1540-1548. (doi:10.2136/sssaj2002.1540)
11. Ma, W. K., Farrell, R. E. & Siciliano, S. D. 2008 Soil formate regulates the fungal nitrous oxide emission pathway. Appl. Environ. Microbiol. 74, 6690-6696. (doi:10. 1128/AEM.00797-08)
12. 2O production by fungal denitrification. Rapid Commun. Mass Spectrom. 22, 3989-3996. (doi:10.1002/rcm.3820)
13. Cathrine, S. J. & Raghukumar, C. 2009 Anaerobic denitrification in fungi from the coastal marine sediments off Goa, India. Mycol. Res. 113, 100-109. (doi:10. 1016/j.mycres.2008.08.009)
14. Kobayashi, M., Matsuo, Y., Takimoto, A., Suzuki, S., Maruo, F. & Shoun, H. 1996 Denitrification, a novel type of respiratory metabolism in fungal mitochondrion. J. Biol. Chem. 271, 16 263-16 267. (doi:10.1074/jbc. 271.27.16263)
15. Uchimura, H., Enjoji, H., Seki, T., Taguchi, A., Takaya, N. & Shoun, H. 2002 Nitrate reductaseformate dehydrogenase couple involved in the fungal denitrification by Fusarium oxysporum. J. Biochem. 131, 579-586.
16. Takaya, N., Kuwazaki, S., Adachi, Y., Suzuki, S., Kikuchi, T., Nakamura, H., Shiro, Y. & Shoun, H. 2003 Hybrid respiration in the denitrifying mitochondria of Fusarium oxysporum. J. Biochem. 133, 461-465. (doi:10.1093/jb/mvg060)
17. Kuwazaki, S., Takaya, N., Nakamura, A. & Shoun, H. 2003 Formate-forming fungal catabolic pathway to supply electrons to nitrate respiration. Biosci. Biotechnol. Biochem. 67, 937-939. (doi:10.1271/bbb.67.937)
18. Zhou, Z., Takaya, N., Nakamura, A., Yamaguchi, M., Takeo, K. & Shoun, H. 2002 Ammonia fermentation, a novel anoxic metabolism of nitrate by fungi. J. Biol. Chem. 277, 1892-1896. (doi:10.1074/jbc.M109096200)
19. Zhou, Z., Takaya, N. & Shoun, H. 2010 Multi-energy metabolic mechanisms of the fungus Fusarium oxysporum in low oxygen environments. Biosci. Biotechnol. Biochem. 74, 2431-2437. (doi:10.1271/bbb.100482)
20. Watsuji, T. O., Takaya, N., Nakamura, A. & Shoun, H. 2003 Denitrification of nitrate by the fungus Cylindrocarpon tonkinense. Biosci. Biotechnol. Biochem. 67, 1115-1120. (doi:10.1271/bbb.67.1115)
21. Watsuji, T. O., Takaya, N., Nakamura, A. & Shoun, H. 2003 A possible role of NADPH-dependent cytochrome P450nor isozyme in glycolysis under denitrifying conditions. Biosci. Biotechnol. Biochem. 67, 1109-1114. (doi:10.1271/bbb.67.1109)
22. Kobayashi, M. & Shoun, H. 1995 The coppercontaining dissimilatory nitrite reductase involved in the denitrifying system of the fungus Fusarium oxysporum. J. Biol. Chem. 270, 4146-4151. (doi:10.1074/ jbc.270.8.4146)
23. Kim, S. W., Fushinobu, S., Zhou, S., Wakagi, T. & Shoun, H. 2009 Eukaryotic nirK genes encoding copper-containing nitrite reductase: originating from the protomitochondrion? Appl. Environ. Microbiol. 75, 2652-2658. (doi:10.1128/AEM.02536-08)
24. Kubota, Y., Takaya, N. & Shoun, H. 1999 Membrane-associated, dissimilatory nitrite reductase of the denitrifying fungus Cylindrocarpon tonkinense. Arch. Microbiol. 171, 210-213. (doi:10.1007/s002 030050701)
25. Tielens, A. G., Rotte, C., van Hellemond, J. J. & Martin, W. 2002 Mitochondria as we don't know them. Trends Biochem. Sci. 27, 564-572. (doi:10.1016/S0968-0004(02)02193-X)
26. Kim, S. W., Fushinobu, S., Zhou, S., Wakagi, T. & Shoun, H. 2010 The possible involvement of coppercontaining nitrite reductase (NirK) and flavohemoglobin in denitrification by the fungus Cylindrocarpon tonkinense. Biosci. Biotechnol. Biochem. 74, 1403-1407. (doi:10. 1271/bbb.100071)
27. Tanimoto, T., Hatano, K., Kim, D. H., Uchiyama, H. & Shoun, H. 1992 Co-denitrification by the denitrifying system of the fungus Fusarium oxysporum. FEMS Microbiol. Lett. 93, 177-180. (doi:10.1016/0378-1097 (92)90525-S)
28. Strous, M., Fuerst, J. A., Kramer, E. H., Logemann, S., Muyzer, G., van de Pas-Schoonen, K. T., Webb, R., Kuenen, J. G. & Jetten, M. S. M. 1999 Missing lithotroph identified as new planctomycete. Nature 400, 446-449. (doi:10.1038/22749)
29. Su, F., Takaya, N. & Shoun, H. 2004 Nitrous oxideforming codenitrification catalyzed by cytochrome P450nor. Biosci. Biotechnol. Biochem. 68, 473-475. (doi:10.1271/bbb.68.473)
30. Shoun, H., Sudo, Y., Seto, Y. & Beppu, T. 1983 Purification and properties of a cytochrome P-450 of a fungus, Fusarium oxysporum. J. Biochem. 94, 1219-1229.
31. Shoun, H., Suyama, W. & Yasui, T. 1989 Soluble, nitrate/nitrite-inducible cytochrome P-450 of the fungus, Fusarium oxysporum. FEBS Lett. 244, 11-14. (doi:10.1016/0014-5793(89)81151-2)
32. Kizawa, H., Tomura, D., Oda, M., Fukamizu, A., Hoshino, T., Gotoh, O., Yasui, T. & Shoun, H. 1991 Nucleotide sequence of the unique nitrate/nitrite-inducible cytochrome P-450 cDNA from Fusarium oxysporum. J. Biol. Chem. 266, 10 632-10 637.
33. Omura, T. 2010 Structural diversity of cytochrome P450 enzyme system. J. Biochem. 147, 297-306. (doi:10.1093/ jb/mvq001)
34. Shiro, Y., Fujii, M., Iizuka, T., Adachi, S., Tsukamoto, K., Nakahara, K. & Shoun, H. 1995 Spectroscopic and kinetic studies on reaction of cytochrome P450nor with nitric oxide. Implication for its nitric oxide reduction mechanism. J. Biol. Chem. 270, 1617-1623. (doi:10. 1074/jbc.270.4.1617)
35. NOR. J. Inorg. Biochem. 88, 343-352. (doi:10. 1016/S0162-0134(01)00386-5)
36. Lehnert, N., Praneeth, V. K. & Paulat, F. 2006 Electronic structure of iron(II)-porphyrin nitroxyl complexes: molecular mechanism of fungal nitric oxide reductase (P450nor). J. Comput. Chem. 27, 1338-1351. (doi:10.1002/jcc.20400)
37. Nakahara, K. & Shoun, H. 1996 N-terminal processing and amino acid sequence of two isoforms of nitric oxide reductase cytochrome P450nor from Fusarium oxysporum. J. Biochem. 120, 1082-1087.
38. Takaya, N., Suzuki, S., Kuwazaki, S., Shoun, H., Maruo, F., Yamaguchi, M. & Takeo, K. 1999 Cytochrome p450nor, a novel class of mitochondrial cytochrome P450 involved in nitrate respiration in the fungus Fusarium oxysporum. Arch. Biochem. Biophys. 372, 340-346. (doi:10.1006/abbi.1999.1499)
39. Kudo, T., Tomura, D., Liu, D. L., Dai, X. Q. & Shoun, H. 1996 Two isozymes of P450nor of Cylindrocarpon tonkinense: molecular cloning of the cDNAs and genes, expressions in the yeast, and the putative NAD(P)Hbinding site. Biochimie 78, 792-799. (doi:10.1016/ S0300-9084(97)82538-2)
40. Usuda, K., Toritsuka, N., Matsuo, Y., Kim, D. H. & Shoun, H. 1995 Denitrification by the fungus Cylindrocarpon tonkinense: anaerobic cell growth and two isozyme forms of cytochrome P-450nor. Appl. Environ. Microbiol. 61, 883-889.
41. Kudo, T., Takaya, N., Park, S. Y., Shiro, Y. & Shoun, H. 2001 A positively charged cluster formed in the heme-distal pocket of cytochrome P450nor is essential for interaction with NADH. J. Biol. Chem. 276, 5020-5026. (doi:10.1074/jbc.M007244200)
42. Zhang, L., Kudo, T., Takaya, N. & Shoun, H. 2002 The B0 helix determines cytochrome P450nor specificity for the electron donors NADH and NADPH. J. Biol. Chem. 277, 33 842-33 847. (doi:10.1074/jbc. M203923200)
43. Oshima, R., Fushinobu, S., Su, F., Zhang, L., Takaya, N. & Shoun, H. 2004 Structural evidence for direct hydride transfer from NADH to cytochrome P450nor. J. Mol. Biol. 342, 207-217. (doi:10.1016/j.jmb.2004.07.009)
44. Umemura, M., Su, F., Takaya, N., Shiro, Y. & Shoun, H. 2004 D88A mutant of cytochrome P450nor provides kinetic evidence for direct complex formation with electron donor NADH. Eur. J. Biochem. 271, 2887-2894. (doi:10.1111/j.1432-1033.2004.04206.x)
45. Shimizu, H., Obayashi, E., Gomi, Y., Arakawa, H., Park, S. Y., Nakamura, H., Adachi, S., Shoun, H. & Shiro, Y. 2000 Proton delivery in NO reduction by fungal nitricoxide reductase. Cryogenic crystallography, spectroscopy, and kinetics of ferric-NO complexes of wild-type and mutant enzymes. J. Biol. Chem. 275, 4816-4826. (doi:10.1074/jbc.275.7.4816)
46. Park, S. Y. et al. 1997 Crystal structure of nitric oxide reductase from denitrifying fungus Fusarium oxysporum. Nat. Struct. Biol. 4, 827-832. (doi:10.1038/ nsb1097-827)
47. Su, F., Fushinobu, S., Takaya, N. &Shoun, H. 2004 Involvement of a Glu71-Arg64 couple in the access channel for NADH in cytochrome p450nor. Biosci. Biotechnol. Biochem. 68, 1156-1159. (doi:10.1271/bbb.68.1156)
48. Nittler, M. P., Hocking-Murray, D., Foo, C. K. & Sil, A. 2005 Identification of Histoplasma capsulatum transcripts induced in response to reactive nitrogen species. Mol. Biol. Cell 16, 4792-4813. (doi:10.1091/mbc. E05-05-0434)
49. Kumon, Y., Sasaki, Y., Kato, I., Takaya, N., Shoun, H. & Beppu, T. 2002 Codenitrification and denitrification are dual metabolic pathways through which dinitrogen evolves from nitrate in Streptomyces antibioticus. J. Bacteriol. 184, 2963-2968. (doi:10.1128/JB.184.11. 2963-2968.2002)