Radical S-adenosylmethionine enzyme catalyzed thioether bond formation in sactipeptide biosynthesis

Current Opinion in Chemical Biology

Volumn 17, Issue 4, 2013, Pages 605-612

  Flühe, Leif ^a   Marahiel, Mohamed A ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE DERIVATIVE; RADICAL; S ADENOSYLMETHIONINE; SACTIPEPTIDE; SULFIDE; UNCLASSIFIED DRUG;

CATALYSIS; CHEMICAL BOND; ELECTRON; GENE CLUSTER; PEPTIDE SYNTHESIS; PRECURSOR; PROTON TRANSPORT; REACTION ANALYSIS; REVIEW; RIBOSOME; SPOROGENESIS;

BIOCATALYSIS; ETHER; FREE RADICALS; PEPTIDES; S-ADENOSYLMETHIONINE; SULFHYDRYL COMPOUNDS;

EID: 84881237635     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2013.06.031     Document Type: Review

References (53)

1. Arnison P.G., Bibb M.J., Bierbaum G., Bowers A.A., Bugni T.S., Bulaj G., Camarero J.A., Campopiano D.J., Challis G.L., Clardy J., et al. Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep 2012, 30:108-160.
2. Murphy K., O'Sullivan O., Rea M.C., Cotter P.D., Ross R.P., Hill C. Genome mining for radical SAM protein determinants reveals multiple sactibiotic-like gene clusters. PLoS ONE 2011, 6:e20852.
3. Babasaki K., Takao T., Shimonishi Y., Kurahashi K. Subtilosin A, a new antibiotic peptide produced by Bacillus subtilis 168: isolation, structural analysis, and biogenesis. J Biochem 1985, 98:585-603.
4. Kawulka K.E., Sprules T., McKay R.T., Mercier P., Diaper C.M., Zuber P., Vederas J.C. Structure of subtilosin A, an antimicrobial peptide from Bacillus subtilis with unusual posttranslational modifications linking cysteine sulfurs to alpha-carbons of phenylalanine and threonine. J Am Chem Soc 2003, 125:4726-4727.
5. Kawulka K.E., Sprules T., Diaper C.M., Whittal R.M., McKay R.T., Mercier P., Zuber P., Vederas J.C. Structure of subtilosin A, a cyclic antimicrobial peptide from Bacillus subtilis with unusual sulfur to alpha-carbon cross-links: formation and reduction of alpha-thio-alpha-amino acid derivatives. Biochemistry 2004, 43:3385-3395.
6. Liu W.-T., Yang Y.-L., Xu Y., Lamsa A., Haste N.M., Yang J.Y., Ng J., Gonzalez D., Ellermeier C.D., Straight P.D., et al. Imaging mass spectrometry of intraspecies metabolic exchange revealed the cannibalistic factors of Bacillus subtilis. Proc Natl Acad Sci U S A 2010, 107:16286-16290.
7. Sit C.S., van Belkum M.J., McKay R.T., Worobo R.W., Vederas J.C. The 3 D solution structure of thurincin H, a bacteriocin with four sulfur to α-carbon crosslinks. Angew Chem Int Ed Engl 2011, 50:8718-8721.
8. Lee H., Churey J.J., Worobo R.W. Biosynthesis and transcriptional analysis of thurincin H, a tandem repeated bacteriocin genetic locus, produced by Bacillus thuringiensis SF361. FEMS Microbiol Lett 2009, 299:205-213.
9. Rea M.C., Sit C.S., Clayton E., O'Connor P.M., Whittal R.M., Zheng J., Vederas J.C., Ross R.P., Hill C. Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. Proc Natl Acad Sci U S A 2010, 107:9352-9357.
10. Sit C.S., McKay R.T., Hill C., Ross R.P., Vederas J.C. The 3D structure of thuricin CD, a two-component bacteriocin with cysteine sulfur to α-carbon cross-links. J Am Chem Soc 2011, 133:7680-7683.
11. Haft D.H., Basu M.K. Biological systems discovery in silico: radical s-adenosylmethionine protein families and their target peptides for posttranslational modification. J Bacteriol 2011, 193:2745-2755.
12. González-Pastor J.E., Hobbs E.C., Losick R. Cannibalism by sporulating bacteria. Science 2003, 301:510-513.
13. Engelberg-Kulka H., Hazan R. Microbiology. Cannibals defy starvation and avoid sporulation. Science 2003, 301:467-468.
14. Rea M.C., Dobson A., O'Sullivan O., Crispie F., Fouhy F., Cotter P.D., Shanahan F., Kiely B., Hill C., Ross R.P. Effect of broad- and narrow-spectrum antimicrobials on Clostridium difficile and microbial diversity in a model of the distal colon. Proc Natl Acad Sci U S A 2011, 108(Suppl 1):4639-4644.
15. Sutyak K.E., Anderson R.A., Dover S.E., Feathergill K.A., Aroutcheva A.A., Faro S., Chikindas M.L. Spermicidal activity of the safe natural antimicrobial peptide subtilosin. Infect Dis Obstet Gynecol 2008, 2008:540758.
16. Silkin L., Hamza S., Kaufman S., Cobb S.L., Vederas J.C. Spermicidal bacteriocins: lacticin 3147 and subtilosin A. Bioorg Med Chem Lett 2008, 18:3103-3106.
17. Shelburne C.E., An F.Y., Dholpe V., Ramamoorthy A., Lopatin D.E., Lantz M.S. The spectrum of antimicrobial activity of the bacteriocin subtilosin A. J Antimicrob Chemother 2007, 59:297-300.
18. Thennarasu S., Lee D.-K., Poon A., Kawulka K.E., Vederas J.C., Ramamoorthy A. Membrane permeabilization, orientation, and antimicrobial mechanism of subtilosin A. Chem Phys Lipids 2005, 137:38-51.
19. Flühe L., Knappe T.A., Gattner M.J., Schäfer A., Burghaus O., Linne U., Marahiel M.A. The radical SAM enzyme AlbA catalyzes thioether bond formation in subtilosin A. Nat Chem Biol 2012, 8:350-357.
20. Flühe L., Burghaus O., Wieckowski B.M., Giessen T.W., Linne U., Marahiel M.A. Two [4Fe-4S] clusters containing radical SAM enzyme SkfB catalyze thioether bond formation during the maturation of the sporulation killing factor. J Am Chem Soc 2013, 135:959-962.
21. Zheng G., Hehn R., Zuber P. Mutational analysis of the sbo-alb locus of Bacillus subtilis: identification of genes required for subtilosin production and immunity. J Bacteriol 2000, 182:3266.
22. Zheng G., Yan L.Z., Vederas J.C., Zuber P. Genes of the sbo-alb locus of Bacillus subtilis are required for production of the antilisterial bacteriocin subtilosin. J Bacteriol 1999, 181:7346-7355.
23. Knerr P.J., van der Donk W.A. Discovery, biosynthesis, and engineering of lantipeptides. Annu Rev Biochem 2012, 81:479-505.
24. Velásquez J.E., van der Donk W.A. Genome mining for ribosomally synthesized natural products. Curr Opin Chem Biol 2011, 15:11-21.
25. Müller W.M., Schmiederer T., Ensle P., Süssmuth R.D. In vitro biosynthesis of the prepeptide of type-III lantibiotic labyrinthopeptin A2 including formation of a CC bond as a post-translational modification. Angew Chem Int Ed Engl 2010, 49:2436-2440.
26. Müller W.M., Ensle P., Krawczyk B., Süssmuth R.D. Leader peptide-directed processing of labyrinthopeptin A2 precursor peptide by the modifying enzyme LabKC. Biochemistry 2011, 50:8362-8373.
27. Aoki M., Ohtsuka T., Yamada M., Ohba Y., Yoshizaki H., Yasuno H., Sano T., Watanabe J., Yokose K., Seto H. Cyclothiazomycin, a novel polythiazole-containing peptide with renin inhibitory activity. Taxonomy, fermentation, isolation and physico-chemical characterization. J Antibiot 1991, 44:582-588.
28. Wang J., Yu Y., Tang K., Liu W., He X., Huang X., Deng Z. Identification and analysis of the biosynthetic gene cluster encoding the thiopeptide antibiotic cyclothiazomycin in Streptomyces hygroscopicus 10-22. Appl Environ Microbiol 2010, 76:2335-2344.
29. Frey P.A., Hegeman A.D., Ruzicka F.J. The radical SAM superfamily. Crit Rev Biochem Mol Biol 2008, 43:63-88.
30. Sofia H., Chen G., Hetzler B., Reyes-Spindola J., Miller N. Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res 2001, 29:1097-1106.
31. Roach P.L. Radicals from S-adenosylmethionine and their application to biosynthesis. Curr Opin Chem Biol 2010, 10.1016/j.cbpa.2010.11.015.
32. Atta M., Arragain S., Fontecave M., Mulliez E., Hunt J.F., Luff J.D., Forouhar F. The methylthiolation reaction mediated by the radical-SAM enzymes. Biochim Biophys Acta 2012, 1824:1223-1230.
33. Lanz N.D., Booker S.J. Identification and function of auxiliary iron-sulfur clusters in radical SAM enzymes. Biochim Biophys Acta 2012, 1824:1196-1212.
34. Peters J.W., Broderick J.B. Emerging paradigms for complex iron-sulfur cofactor assembly and insertion. Annu Rev Biochem 2012, 81:429-450.
35. Wiig J.A., Hu Y., Lee C.C., Ribbe M.W. Radical SAM-dependent carbon insertion into the nitrogenase M-cluster. Science 2012, 337:1672-1675.
36. Pierre S., Guillot A., Benjdia A., Sandström C., Langella P., Berteau O. Thiostrepton tryptophan methyltransferase expands the chemistry of radical SAM enzymes. Nat Chem Biol 2012, 8:957-959.
37. Mehta A.P., Hanes J.W., Abdelwahed S.H., Hilmey D.G., Hänzelmann P., Begley T.P. Catalysis of a new ribose carbon-insertion reaction by the molybdenum cofactor biosyn-thetic enzyme MoaA. Biochemistry 2013, 10.1021/bi3016026.
38. Nicolet Y., Amara P., Mouesca J.-M., Fontecilla-Camps J.C. Unexpected electron transfer mechanism upon AdoMet cleavage in radical SAM proteins. Proc Natl Acad Sci U S A 2009, 106:14867-14871.
39. Haft D.H. Bioinformatic evidence for a widely distributed, ribosomally produced electron carrier precursor, its maturation proteins, and its nicotinoprotein redox partners. BMC Genomics 2011, 12:21.
40. Grove T.L., Ahlum J.H., Sharma P., Krebs C., Booker S.J. A consensus mechanism for radical SAM-dependent dehydrogenation? BtrN contains two [4Fe-4S] clusters. Biochemistry 2010, 49:3783-3785.
41. Grove T.L., Lee K.-H., St Clair J., Krebs C., Booker S.J. In vitro characterization of AtsB, a radical SAM formylglycine-generating enzyme that contains three [4Fe-4S] clusters. Biochemistry 2008, 47:7523-7538.
42. Guianvarc'h D., Florentin D., Tse Sum Bui B., Nunzi F., Marquet A. Biotin synthase, a new member of the family of enzymes which uses S-adenosylmethionine as a source of deoxyadenosyl radical. Biochem Biophys Res Commun 1997, 236:402-406.
43. Anton B.P., Saleh L., Benner J.S., Raleigh E.A., Kasif S., Roberts R.J. RimO, a MiaB-like enzyme, methylthiolates the universally conserved Asp88 residue of ribosomal protein S12 in Escherichia coli. Proc Natl Acad Sci U S A 2008, 105:1826-1831.
44. Anton B.P., Russell S.P., Vertrees J., Kasif S., Raleigh E.A., Limbach P.A., Roberts R.J. Functional characterization of the YmcB and YqeV tRNA methylthiotransferases of Bacillus subtilis. Nucleic Acids Res 2010, 38:6195-6205.
45. Pierrel F., Douki T., Fontecave M., Atta M. MiaB protein is a bifunctional radical-S-adenosylmethionine enzyme involved in thiolation and methylation of tRNA. J Biol Chem 2004, 279:47555-47563.
46. Roach P.L., Clifton I.J., Hensgens C.M., Shibata N., Schofield C.J., Hajdu J., Baldwin J.E. Structure of isopenicillin N synthase complexed with substrate and the mechanism of penicillin formation [Internet]. Nature 1997, 387:827-830.
47. Ugulava N.B., Gibney B.R., Jarrett J.T. Biotin synthase contains two distinct iron-sulfur cluster binding sites: chemical and spectroelectrochemical analysis of iron-sulfur cluster interconversions. Biochemistry 2001, 40:8343-8351.
48. Jameson G.N.L., Cosper M.M., Hernández H.L., Johnson M.K., Huynh B.H. Role of the [2Fe-2S] cluster in recombinant Escherichia coli biotin synthase. Biochemistry 2004, 43:2022-2031.
49. Ugulava N.B., Sacanell C.J., Jarrett J.T. Spectroscopic changes during a single turnover of biotin synthase: destruction of a [2Fe-2S] cluster accompanies sulfur insertion. Biochemistry 2001, 40:8352-8358.
50. Lee K.-H., Saleh L., Anton B.P., Madinger C.L., Benner J.S., Iwig D.F., Roberts R.J., Krebs C., Booker S.J. Characterization of RimO, a new member of the methylthiotransferase subclass of the radical SAM superfamily. Biochemistry 2009, 48:10162-10174.
51. Arragain S., Handelman S.K., Forouhar F., Wei F.-Y., Tomizawa K., Hunt J.F., Douki T., Fontecave M., Mulliez E., Atta M. Identification of eukaryotic and prokaryotic methylthiotransferase for biosynthesis of 2-methylthio-N6-threonylcarbamoyladenosine in tRNA. J Biol Chem 2010, 285:28425-28433.
52. Forouhar F., Arragain S., Atta M., Gambarelli S., Mouesca J.-M., Hussain M., Xiao R., Kieffer-Jaquinod S., Seetharaman J., Acton T.B., et al. Two Fe-S clusters catalyze sulfur insertion by radical-SAM methylthiotransferases. Nat Chem Biol 2013, 10.1038/nchembio.1229.
53. Baldwin J.E., Bradley M. Isopenicillin N synthase: mechanistic studies. Chem Rev 1990, 90:1079-1088.