A Novel Cysteine Desulfurase Influencing Organosulfur Compounds in Lentinula Edodes

Overview

Journal Sci Rep

Specialty Science

Date 2015 Jun 10

PMID 26054293

Citations 13

Authors

Ying Liu

Xiao-Yu Lei

Lian-Fu Chen

Yin-Bing Bian

Hong Yang

Salam A Ibrahim

Wen Huang

Affiliations

Soon will be listed here.

Abstract

Organosulfur compounds are the basis for the unique aroma of Lentinula edodes, and cysteine sulfoxide lyase (C-S lyase) is the key enzyme in this trait. The enzyme from Alliium sativum has been crystallized and well-characterized; however, there have been no reports of the characterization of fungi C-S lyase at the molecular level. We identified a L. edodes C-S lyase (Lecsl), cloned a gene of Csl encoded Lecsl and then combined modeling, simulations, and experiments to understand the molecular basis of the function of Lecsl. Our analysis revealed Lecsl to be a novel cysteine desulfurase and not a type of cysteine sulfoxide lyase. The pyridoxal-5-phosphate (PLP) molecule bonded tightly to Lecsl to form a Lecsl-PLP complex. Moreover, the Lecsl had one active center that served to bind two kinds of substrates, S-methyl-L-cysteine sulfoxide and L-cysteine, and had both cysteine sulfoxide lyase and cysteine desulfurase activity. We found that the amino acid residue Asn393 was essential for the catalytic activity of Lecsl and that the gene Csl encoded a novel cysteine desulfurase to influence organosulfur compounds in L. edodes. Our results provide a new insight into understanding the formation of the unique aroma of L. edodes.

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References

Poliak P, Van Hoewyk D, Obornik M, Zikova A, Stuart K, Tachezy J . Functions and cellular localization of cysteine desulfurase and selenocysteine lyase in Trypanosoma brucei. FEBS J. 2009; 277(2):383-93. PMC: 2813251. DOI: 10.1111/j.1742-4658.2009.07489.x. View

Rabinkov A, Zhu X, Grafi G, Galili G, Mirelman D . Alliin lyase (Alliinase) from garlic (Allium sativum). Biochemical characterization and cDNA cloning. Appl Biochem Biotechnol. 1994; 48(3):149-71. DOI: 10.1007/BF02788739. View

Kusterer J, Keusgen M . Cysteine sulfoxides and volatile sulfur compounds from Allium tripedale. J Agric Food Chem. 2009; 58(2):1129-37. DOI: 10.1021/jf903581f. View

Renard M, Fersht A . Anomalous pH dependence of kcat-KM in enzyme reactions. Rate constants for the association of chymotrypsin with substrates. Biochemistry. 1973; 12(23):4713-8. DOI: 10.1021/bi00747a026. View

Shimada S, Komamura K, Kumagai H, Sakurai H . Inhibitory activity of shiitake flavor against platelet aggregation. Biofactors. 2005; 22(1-4):177-9. DOI: 10.1002/biof.5520220136. View

Kim S, Park S . Structural changes during cysteine desulfurase CsdA and sulfur acceptor CsdE interactions provide insight into the trans-persulfuration. J Biol Chem. 2013; 288(38):27172-27180. PMC: 3779715. DOI: 10.1074/jbc.M113.480277. View

Toney M . Reaction specificity in pyridoxal phosphate enzymes. Arch Biochem Biophys. 2004; 433(1):279-87. DOI: 10.1016/j.abb.2004.09.037. View

Mihara H, Kurihara T, Yoshimura T, Soda K, Esaki N . Cysteine sulfinate desulfinase, a NIFS-like protein of Escherichia coli with selenocysteine lyase and cysteine desulfurase activities. Gene cloning, purification, and characterization of a novel pyridoxal enzyme. J Biol Chem. 1997; 272(36):22417-24. DOI: 10.1074/jbc.272.36.22417. View

Shimon L, Rabinkov A, Shin I, Miron T, Mirelman D, Wilchek M . Two structures of alliinase from Alliium sativum L.: apo form and ternary complex with aminoacrylate reaction intermediate covalently bound to the PLP cofactor. J Mol Biol. 2006; 366(2):611-25. DOI: 10.1016/j.jmb.2006.11.041. View

10.

Kuettner E, Hilgenfeld R, Weiss M . The active principle of garlic at atomic resolution. J Biol Chem. 2002; 277(48):46402-7. DOI: 10.1074/jbc.M208669200. View

11.

Kitamura N, Shimomura N, ISEKI J, Honma M, Chiba S, Tahara S . Cysteine-S-conjugate beta-lyase activity and pyridoxal phosphate binding site of onion alliin lyase. Biosci Biotechnol Biochem. 1997; 61(8):1327-30. DOI: 10.1271/bbb.61.1327. View

12.

Jacob C, Giles G, Giles N, Sies H . Sulfur and selenium: the role of oxidation state in protein structure and function. Angew Chem Int Ed Engl. 2003; 42(39):4742-58. DOI: 10.1002/anie.200300573. View

13.

Grishin N, Phillips M, Goldsmith E . Modeling of the spatial structure of eukaryotic ornithine decarboxylases. Protein Sci. 1995; 4(7):1291-304. PMC: 2143167. DOI: 10.1002/pro.5560040705. View

14.

Zheng L, White R, Cash V, Dean D . Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. Biochemistry. 1994; 33(15):4714-20. DOI: 10.1021/bi00181a031. View

15.

Kumagai H, Kono H, Sakurai H, Tokimoto K . Comparison of C-S lyase in Lentinus edodes and Allium sativum. Biosci Biotechnol Biochem. 2003; 66(12):2560-6. DOI: 10.1271/bbb.66.2560. View

16.

Ouzounis C, Sander C . Homology of the NifS family of proteins to a new class of pyridoxal phosphate-dependent enzymes. FEBS Lett. 1993; 322(2):159-64. DOI: 10.1016/0014-5793(93)81559-i. View

17.

Kappes B, Tews I, Binter A, Macheroux P . PLP-dependent enzymes as potential drug targets for protozoan diseases. Biochim Biophys Acta. 2011; 1814(11):1567-76. DOI: 10.1016/j.bbapap.2011.07.018. View

18.

Pandey A, Golla R, Yoon H, Dancis A, Pain D . Persulfide formation on mitochondrial cysteine desulfurase: enzyme activation by a eukaryote-specific interacting protein and Fe-S cluster synthesis. Biochem J. 2012; 448(2):171-87. DOI: 10.1042/BJ20120951. View

19.

Mihara H, Fujii T, Kato S, Kurihara T, Hata Y, Esaki N . Structure of external aldimine of Escherichia coli CsdB, an IscS/NifS homolog: implications for its specificity toward selenocysteine. J Biochem. 2002; 131(5):679-85. DOI: 10.1093/oxfordjournals.jbchem.a003151. View

20.

Lancaster J, Shaw M, Joyce M, McCallum J, McManus M . A novel alliinase from onion roots. Biochemical characterization and cDNA cloning. Plant Physiol. 2000; 122(4):1269-79. PMC: 58963. DOI: 10.1104/pp.122.4.1269. View