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DOI: 10.1055/s-0036-1588526
Fungal Dihydroxynaphthalene-Melanin: Diversity-Oriented Biosynthesis through Enzymatic and Non-enzymatic Transformations
S.M.H. is grateful to the Council of Scientific and Industrial Research, New Delhi [Project No. 02(0258)/16/EMR-II] and SERB-DST (YSS/2014/000792) for fundingPublikationsverlauf
Received: 20. Mai 2017
Accepted after revision: 03. Juli 2017
Publikationsdatum:
31. August 2017 (online)
Abstract
Tetrahydroxynaphthalene reductase (T4HNR) from Magnaporthe grisea catalyzes the reduction of polyhydroxynaphthalenes, hydroxynaphthoquinones, and 1,4-diketones, with extensive ramifications for the biosynthesis of (shunt) metabolites related to 1,8-dihydroxynaphthalene (DHN)-melanin biosynthesis. Hence, an extended model for DHN-melanin biosynthesis has been developed which is based on a screening hypothesis involving non-enzymatic transformations such as oxidations and tautomerism. This has led to the broadening of the functions of several short-chain dehydrogenases/reductases (SDRs) capable of reducing polyhydroxyanthracenes, polyhydroxynaphthalenes, and polyhydroxybenzenes. Our work, broadening the scope of enzymatic dearomatization reactions, provides access to the biocatalytic synthesis of a variety of natural and natural-like products. Furthermore, the results described in this account provide the basis for the identification of other SDRs amenable to reducing aromatic compounds, and thus enable the identification of biosynthetic gene clusters most likely involved in the biosynthesis of aromatic polyketides.
1 Introduction
2 Biosynthesis of 1,8-Dihydroxynaphthalene (DHN)
3 Biosynthesis of Shunt Metabolites and the Origin of Molecular Diversity
3.1 Role of Spontaneous Non-enzymatic Oxidations
3.2 Role of T4HNR and T3HNR
3.3 Role of Tautomerism in the Biosynthesis of (Shunt) Metabolites
4 Extended Melanin Biosynthesis: A Screening Hypothesis
5 Useful Outcomes of the Newly Identified Melanin Biosynthetic Pathway
5.1 NADP+ Regeneration Using Lawsone as Mediator
5.2 Anthrahydroquinone as an Intermediate in the Biosynthesis of Chrysophanol and Other Anthraquinone-Derived Products
5.3 Combination of T3HNR and GDH To Access trans-Ketodiols
5.4 Phloroglucinol Reductases (PGRs) To Dearomatize Monomeric Phenols
6 Conclusion
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References
- 1 Bell AA. Wheeler MH. Annu. Rev. Phytopathol. 1986; 24: 411
- 2 Butler MJ. Day AW. Can. J. Microbiol. 1998; 44: 1115
- 3 Henson JM. Butler MJ. Day AW. Annu. Rev. Phytopathol. 1999; 37: 447
- 4 Plonka PM. Grabacka M. Acta. Biochim. Pol. 2006; 53: 429
- 5 Gao Q. Garcia-Pichel F. Nat. Rev. Microbiol. 2011; 9: 791
- 6 Eisenman HC. Casadevall A. Appl. Microbiol. Biotechnol. 2012; 93: 931
- 7 Langfelder K. Streibel M. Jahn B. Haase G. Brakhage A. Fungal Genet. Biol. 2003; 38: 143
- 8 Prota G. d’Ischia M. Napolitano A. The Pigmentary System: Physiology and Pathophysiology . Oxford University Press; New York: 1998. 1st ed. 307
- 9 Guo CJ. Sun W.-W. Bruno KS. Oakley BR. Kellerd NP. Wang C. Chem. Sci. 2015; 6: 5913
- 10 Geib E. Gressler M. Viediernikova I. Hillmann F. Jacobsen ID. Nietzsche S. Hertweck C. Brock M. Cell Chem. Biol. 2016; 23: 1
- 11 Bell AA. Stipanovic RD. Puhalla JE. Tetrahedron 1976; 32: 1353
- 12 Bell AA. Puhalla JE. Tolmsoff WJ. Stipanovic RD. Can. J. Microbiol. 1976; 22: 787
- 13 Wheeler MH. Trans. Br. Mycol. Soc. 1983; 81: 29
- 14 Geis PA. Wheeler MH. Szaniszlo PJ. Arch. Microbiol. 1984; 137: 324
- 15 Wheeler MH. Stipanovic RD. Arch. Microbiol. 1985; 142: 234
- 16 Taylor BE. Wheeler MH. Szaniszlo PJ. Mycologia 1987; 79: 320
- 17 Wheeler MH. Abramczyk D. Puckhaber LS. Naruse M. Ebizuka Y. Fujii I. Szaniszlo PJ. Eukaryot. Cell. 2008; 7: 1699
- 18 Okuno T. Matsuura K. Furusawa I. J. Pestic. Sci. 1983; 8: 357
- 19 Woloshuk CP. Sisler HD. Tokousbalides MC. Dutky SR. Pestic. Biochem. Physiol. 1980; 14: 256
- 20 Fujii I. Mori Y. Watanabe A. Kubo Y. Tsuji G. Ebizuka Y. Biosci. Biotechnol. Biochem. 1999; 63: 1445
- 21 Fujii I. Mori Y. Watanabe A. Kubo Y. Tsuji G. Ebizuka Y. Biochemistry 2000; 39: 8853
- 22 Vagstad AL. Hill EA. Labonte JW. Townsend CA. Chem. Biol. 2012; 19: 1525
- 23 Fujii I. Yasuoka Y. Tsai HF. Chang YC. Kwon-Chung KJ. Ebizuka Y. J. Biol. Chem. 2004; 279: 44613
- 24 Tsai HF. Fujii I. Watanabe A. Wheeler MH. Chang YC. Yasuoka Y. Ebizuka Y. Kwon-Chung KJ. J. Biol. Chem. 2001; 276: 29292
- 25 Watanabe A. Fujii I. Tsai HF. Chang YC. Kwon-Chung KJ. Ebizuka Y. FEMS Microbiol. Lett. 2000; 192: 39
- 26 Watanabe A. Fujii I. Sankawa U. Mayorga ME. Timberlake WE. Ebizuka Y. Tetrahedron Lett. 1999; 40: 91
- 27 Feng B. Wang X. Hauser M. Kaufmann S. Jentsch S. Haase G. Becker JM. Szaniszlo PJ. Infect. Immun. 2001; 69: 1781
- 28 Casadevall A. Nakouzi A. Crippa PR. Eisner M. PLoS one 2012; 7: e30299
- 29 Nosanchuk JD. Stark RE. Casadevall A. Front. Microbiol. 2016; 6: 1463
- 30 Viviani F. Gaudry M. Marquet A. J. Chem. Soc., Perkin Trans. 1 1990; 5: 1255
- 31 Vidal-Cros A. Viviani F. Labesse G. Boccara M. Gaudry M. Eur. J. Biochem. 1994; 219: 985
- 32 Thompson JE. Fahnestock S. Farrall L. Liao DI. Valent B. Jordan DB. J. Biol. Chem. 2000; 275: 34867
- 33 Dean RA. Talbot NJ. Ebbole DJ. Farman ML. Mitchell TK. Orbach MJ. Thon M. Kulkarni R. Xu JR. Pan H. Read ND. Lee YH. Carbone I. Brown D. Oh YY. Donofrio N. Jeong JS. Soanes DM. Djonovic S. Kolomiets E. Rehmeyer C. Li W. Harding M. Kim S. Lebrun MH. Bohnert H. Coughlan S. Butler J. Calvo S. Ma LJ. Nicol R. Purcell S. Nusbaum C. Galagan JE. Birren BW. Nature 2005; 434: 980
- 34 Schätzle MA. Flemming S. Husain SM. Richter M. Günther S. Müller M. Angew. Chem. Int. Ed. 2012; 51: 2643
- 35 Liao DI. Thompson JE. Fahnestock S. Valent B. Jordan DB. Biochemistry 2001; 40: 8696
- 36 Husain SM. Schätzle MA. Röhr C. Lüdeke S. Müller M. Org. Lett. 2012; 14: 3600
- 37 Husain SM. Schätzle MA. Lüdeke S. Müller M. Angew. Chem. Int. Ed. 2014; 53: 9806
- 38 Conradt D. Schätzle MA. Husain SM. Müller M. ChemCatChem. 2015; 7: 3116
- 39 McGovern EP. Bentley R. Biochemistry 1975; 14: 3138
- 40 Funa N. Funabashi M. Yoshimura E. Horinouchi S. J. Biol. Chem. 2005; 280: 14514
- 41 Munday R. Methods Enzymol. 2004; 382: 364
- 42 Dickinson BC. Chang CJ. Nat. Chem. Biol. 2011; 7: 504
- 43 Yeo WH. Yun BS. Kim SS. Park EK. Kim YH. Yoo ID. Yu SH. J. Antibiot. 1998; 51: 952
- 44 Maskey RP. Fotso S. Lessmann H. Grün-Wollny I. Lackner H. Laatsch H. Z. Naturforsch. 2005; 60: 183
- 45 Abdalla MA. Win HY. Islam MT. Tiedemann AV. Schüffler A. Laatsch H. J. Antibiot. 2011; 64: 655
- 46 Yamashita M. Kaneko M. Tokuda H. Nishimura K. Kumeda Y. Iida A. Bioorg. Med. Chem. 2009; 17: 6286
- 47 Bonifazi EL. Ríos-Luci C. León LG. Burton G. Padrón JM. Misico RI. Bioorg. Med. Chem. 2010; 18: 2621
- 48 Abou-Mansour E. Couché E. Tabacchi R. Phytopathol. Mediterr. 2004; 43: 75
- 49 Barnes EC. Jumpathong J. Lumyong S. Voigt K. Hertweck C. Chem. Eur. J. 2016; 22: 4551
- 50 Simpson TJ. Weerasooriya MK. B. J. Chem. Soc., Perkin Trans. 1 2000; 16: 2771
- 51 Kihara J. Moriwaki A. Ueno M. Tokunaga T. Arase S. Honda Y. Curr. Genet. 2004; 45: 197
- 52 Tianero MD. Pierce E. Raghuraman S. Sardar D. McIntosh JA. Heemstra JR. Schonrock Z. Covington BC. Maschek JA. Cox JE. Bachmann BO. Olivera BM. Ruffner DE. Schmidt EW. Proc. Natl. Acad. Sci. U.S.A. 2016; 113: 1772
- 53 Firn RD. Jones CG. Nat. Prod. Rep. 2003; 20: 382
- 54 Haas J. Schätzle MA. Husain SM. Schulz-Fincke J. Jung M. Hummel W. Müller M. Lüdeke S. Chem. Commun. 2016; 52: 5198
- 55 Schätzle MA. Husain SM. Ferlaino S. Müller M. J. Am. Chem. Soc. 2012; 134: 14742
- 56 Broadbent AD. Sommermann EF. J. Chem. Soc. B 1967; 376
- 57 Broadbent AD. Sommermann EF. J. Chem. Soc. B 1968; 519
- 58 Broadbent AD. Sommermann EF. J. Chem. Soc. B 1968; 1144
- 59 Bredereck K. Sommermann F. Diamantoglou M. Chem. Ber. 1969; 102: 1053
- 60 Bredereck K. Diamantoglou M. Sommermann F. Chem. Ber. 1970; 103: 1748
- 61 Conradt D. Schätzle MA. Haas J. Townsend CA. Müller M. J. Am. Chem. Soc. 2015; 137: 10867
- 62 Fürtges L. Conradt D. Schätzle MA. Singh SK. Kraševec N. Rižner TL. Müller M. Husain SM. ChemBioChem 2016; 18: 77
- 63 Zhang Z. Gong Y.-K. Zhou Q. Hu Y. Ma H.-M. Chen Y.-S. Igarashi Y. Pan L. Tang G.-L. Proc. Natl. Acad. Sci. U.S.A. 2017; 114: 1554
- 64 Cai Y.-S. Guo Y.-W. Krohn K. Nat. Prod. Rep. 2010; 27: 1840
- 65 Andolfi A. Maddau L. Cimmino A. Linaldeddu BT. Franceschini A. Serra S. Basso S. Melck D. Evidente A. J. Nat. Prod. 2012; 75: 1785
- 66 Conradt D. Hermann B. Gerhardt S. Einsle O. Müller M. Angew. Chem. Int. Ed. 2016; 55: 15531
- 67 Pittayakhajonwut P. Sohsomboon P. Dramae A. Suvannakad R. Lapanun S. Tantichareon M. Planta Med. 2008; 74: 281
- 68 Kavanagh KL. Jörnvall H. Persson B. Oppermann U. Cell Mol. Life Sci. 2008; 65: 3895
- 69 Ebert B. Kisiela M. Maser E. Biol. Rev. 2015; 90: 254