Restoration of bioactive lantibiotic suicin from a remnant lan locus of pathogenic Streptococcus suis serotype 2

Applied and Environmental Microbiology

Volumn 80, Issue 3, 2014, Pages 1062-1071

  Wang, Jian ^a,b   Gao, Yong ^a,b   Teng, Kunling ^a   Zhang, Jie ^a   Sun, Shutao ^a   Zhong, Jin ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL PEPTIDE; BACTERICIDAL ACTIVITY; FRAME-SHIFT MUTATION; GRAM-POSITIVE BACTERIUM; GRAM-POSITIVE STRAINS; LACTOCOCCUS LACTIS; STREPTOCOCCUS SUIS SEROTYPE 2; VANCOMYCIN-RESISTANT ENTEROCOCCI;

BIOCHEMISTRY; BIOSYNTHESIS; COVALENT BONDS; ESCHERICHIA COLI; PLANTS (BOTANY);

GENES;

AMINO ACID; ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOACTIVITY; PATHOGEN; PATHOGENICITY; PEPTIDE; VIRULENCE;

BACTERIOCIN;

ARTICLE; BIOLOGY; BIOSYNTHESIS; DRUG EFFECT; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; GRAM POSITIVE BACTERIUM; METABOLISM; MICROBIAL VIABILITY; STREPTOCOCCUS SUIS;

BACTERIOCINS; BIOSYNTHETIC PATHWAYS; COMPUTATIONAL BIOLOGY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GRAM-POSITIVE BACTERIA; MICROBIAL VIABILITY; STREPTOCOCCUS SUIS;

EID: 84893016146     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03213-13     Document Type: Article

References (48)

1. Hancock RE, Sahl H-G. 2006. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 24:1551-1557. http://dx.doi.org/10.1038/nbt1267.
2. Piper C, Cotter PD, Ross RP, Hill C. 2009. Discovery of medically significant lantibiotics. Curr. Drug Discov. Technol. 6:1-18. http://dx.doi .org/10.2174/157016309787581075.
3. van Heel AJ, Montalban-Lopez M, Kuipers OP. 2011. Evaluating the feasibility of lantibiotics as an alternative therapy against bacterial infections in humans. Expert Opin. Drug Metab. Toxicol. 7:675-680. http://dx .doi.org/10.1517/17425255.2011.573478.
4. Chatterjee C, Paul M, Xie L, van der Donk WA. 2005. Biosynthesis and mode of action of lantibiotics. Chem. Rev. 105:633-684. http://dx.doi.org /10.1021/cr030105v.
5. Jung G. 1991. Lantibiotics-ribosomally synthesized biologically active polypeptides containing sulfide bridges and α,β-didehydroamino acids. Angew. Chem. Int. Ed. Engl. 30:1051-1068. http://dx.doi.org/10.1002/anie.199110513.
6. Koponen O, Tolonen M, Qiao M, Wahlström G, Helin J, Saris PE. 2002. NisB is required for the dehydration and NisC for the lanthionine formation in the post-translational modification of nisin. Microbiology 148(Pt 11):3561-3568.
7. Chatterjee C, Miller LM, Leung YL, Xie L, Yi M, Kelleher NL, van der Donk WA. 2005. Lacticin 481 synthetase phosphorylates its substrate during lantibiotic production. J. Am. Chem. Soc. 127:15332-15333. http: //dx.doi.org/10.1021/ja0543043.
8. Håvarstein LS, Diep DB, Nes IF. 1995. A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export. Mol. Microbiol. 16:229-240. http://dx.doi.org/10.1111/j.13652958.1995.tb02295.x.
9. Twomey D, Ross R, Ryan M, Meaney B, Hill C. 2002. Lantibiotics produced by lactic acid bacteria: structure, function and applications. Antonie Van Leeuwenhoek 82:165-185. http://dx.doi.org/10.1023/A:1020660321724.
10. Daly M, Cotter KPD, Hill C, Ross RP. 2012. Lantibiotic production by pathogenic microorganisms. Curr. Protein Pept. Sci. 13:509-523. http: //dx.doi.org/10.2174/138920312803582997.
11. Coburn PS, Gilmore MS. 2003. The Enterococcus faecalis cytolysin: a novel toxin active against eukaryotic and prokaryotic cells. Cell. Microbiol. 5:661-669. http://dx.doi.org/10.1046/j.1462-5822.2003.00310.x.
12. Nes IF, Diep DB, Holo H. 2007. Bacteriocin diversity in Streptococcus and Enterococcus. J. Bacteriol. 189:1189-1198. http://dx.doi.org/10.1128/JB.01254-06.
13. Majchrzykiewicz JA, Lubelski J, Moll GN, Kuipers A, Bijlsma JJ, Kuipers OP, Rink R. 2010. Production of a class II two-component lantibiotic of Streptococcus pneumoniae using the class I nisin synthetic machinery and leader sequence. Antimicrob. Agents Chemother. 54: 1498-1505. http://dx.doi.org/10.1128/AAC.00883-09.
14. Begley M, Cotter PD, Hill C, Ross RP. 2009. Identification of a novel two-peptide lantibiotic, lichenicidin, following rational genome mining for LanM proteins. Appl. Environ. Microbiol. 75:5451-5460. http://dx.doi .org/10.1128/AEM.00730-09.
15. van Heel AJ, de Jong A, Montalban-Lopez M, Kok J, Kuipers OP. 15 May 2013. BAGEL3: automated identification of genes encoding bacteriocins and (non-)bactericidal posttranslationally modified peptides. Nucleic Acids Res. 41:W448-W453. http://dx.doi.org/10.1093/nar/gkt391.
16. Marsh A, O'Sullivan O, Ross RP, Cotter P, Hill C. 2010. In silico analysis highlights the frequency and diversity of type 1 lantibiotic gene clusters in genome sequenced bacteria. BMC Genomics 11:679. http://dx.doi.org/10.1186/1471-2164-11-679.
17. Daly KM, Upton M, Sandiford SK, Draper LA, Wescombe PA, Jack RW, O'Connor PM, Rossney A, Götz F, Hill C. 2010. Production of the Bsa lantibiotic by community-acquired Staphylococcus aureus strains. J. Bacteriol. 192:1131-1142. http://dx.doi.org/10.1128/JB.01375-09.
18. Tang JQ, Wang CJ, Feng YJ, Yang WZ, Song HD, Chen ZH, Yu HJ, Pan XZ, Zhou XJ, Wang HR, Wu B, Wang HL, Zhao HM, Lin Y, Yue JH, Wu ZQ, He XW, Gao F, Khan AH, Wang J, Zhao GP, Wang Y, Wang X, Chen Z, Gao GF. 2006. Streptococcal toxic shock syndrome caused by Streptococcus suis serotype 2. PLoS Med. 3:e151. http://dx.doi.org/10.1371 /journal.pmed.0030151.
19. Normile D. 2005. Infectious diseases-WHO probes deadliness of China's pig-borne disease. Science 309:1308-1309. http://dx.doi.org/10.1126 /science.309.5739.1308a.
20. Chen C, Tang J, Dong W, Wang C, Feng Y, Wang J, Zheng F, Pan X, Liu D, Li M. 2007. A glimpse of streptococcal toxic shock syndrome from comparative genomics of S. suis 2 Chinese isolates. PLoS One 2:e315. http: //dx.doi.org/10.1371/journal.pone.0000315.
21. Li M, Wang C, Feng Y, Pan X, Cheng G, Wang J, Ge J, Zheng F, Cao M, Dong Y, Liu D, Lin Y, Du H, Gao GF, Wang X, Hu F, Tang J. 2008. SalK/SalR, a two-component signal transduction system, is essential for full virulence of highly invasive Streptococcus suis serotype 2. PLoS One 3:e2080. http://dx.doi.org/10.1371/journal.pone.0002080.
22. Holden MT, Hauser H, Sanders M, Ngo TH, Cherevach I, Cronin A, Goodhead I, Mungall K, Quail MA, Price C, Rabbinowitsch E, Sharp S, Croucher NJ, Chieu TB, Mai NT, Diep TS, Chinh NT, Kehoe M, Leigh JA, Ward PN, Dowson CG, Whatmore AM, Chanter N, Iversen P, Gottschalk M, Slater JD, Smith HE, Spratt BG, Xu J, Ye C, Bentley S, Barrell BG, Schultsz C, Maskell DJ, Parkhill J. 2009. Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen Streptococcus suis. PLoS One 4:e6072. http://dx.doi.org /10.1371/journal.pone.0006072.
23. Sambrook J, Fritsch E, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Ni J, Teng K, Liu G, Qiao C, Huan L, Zhong J. 2011. Autoregulation of lantibiotic bovicin HJ50 biosynthesis by the BovK-BovR two-component signal transduction system in Streptococcus bovis HJ50. Appl. Environ. Microbiol. 77:407-415. http://dx.doi.org/10.1128/AEM.01278-10.
25. Chiu J, March PE, Lee R, Tillett D. 2004. Site-directed, ligase-independent mutagenesis (SLIM): a single-tube methodology approaching 100% efficiency in 4h. Nucleic Acids Res. 32:e174-e174. http://dx.doi.org/10.1093/nar/gnh172.
26. Schägger H. 2006. Tricine-SDS-PAGE. Nat. Protoc. 1:16-22. http://dx .doi.org/10.1038/nprot.2006.4.
27. Sun Z, Zhong J, Liang X, Liu J, Chen X, Huan L. 2009. Novel mechanism for nisin resistance via proteolytic degradation of nisin by the nisin resistance protein NSR. Antimicrob. Agents Chemother. 53:1964-1973. http://dx.doi.org/10.1128/AAC.01382-08.
28. Levengood MR, Knerr PJ, Oman TJ, van der Donk WA. 2009. In vitro mutasynthesis of lantibiotic analogues containing nonproteinogenic amino acids. J. Am. Chem. Soc. 131:12024-12025. http://dx.doi.org/10.1021/ja903239s.
29. Schneider T, Kruse T, Wimmer R, Wiedemann I, Sass V, Pag U, Jansen A, Nielsen AK, Mygind PH, Raventos DS, Neve S, Ravn B, Bonvin AM, De Maria L, Andersen AS, Gammelgaard LK, Sahl HG, Kristensen HH. 2010. Plectasin, a fungal defensin, targets the bacterial cell wall precursor lipid II. Science 328:1168-1172. http://dx.doi.org /10.1126/science.1185723.
30. Holo H, Nes IF. 1995. Transformation of Lactococcus by electroporation. Methods Mol. Biol. 47:195-199.
31. Upton M, Tagg J, Wescombe P, Jenkinson H. 2001. Intra- and interspecies signaling between Streptococcus salivarius and Streptococcus pyogenes mediated by SalA and SalA1 lantibiotic peptides. J. Bacteriol. 183:3931-3938. http://dx.doi.org/10.1128/JB.183.13.3931-3938.2001.
32. Liu G, Zhong J, Ni J, Chen M, Xiao H, Huan L. 2009. Characteristics of the bovicin HJ50 gene cluster in Streptococcus bovis HJ50. Microbiology 155:584-593. http://dx.doi.org/10.1099/mic.0.022707-0.
33. Kabuki T, Uenishi H, Seto Y, Yoshioka T, Nakajima H. 2009. A unique lantibiotic, thermophilin 1277, containing a disulfide bridge and two thioether bridges. J. Appl. Microbiol. 106:853-862. http://dx.doi.org/10.1111/j.1365-2672.2008.04059.x.
34. Kabuki T, Kawai Y, Uenishi H, Seto Y, Kok J, Nakajima H, Saito T. 2011. Gene cluster for biosynthesis of thermophilin 1277-a lantibiotic produced by Streptococcus thermophilus SBT1277, and heterologous expression of TepI, a novel immunity peptide. J. Appl. Microbiol. 110:641-649. http://dx.doi.org/10.1111/j.1365-2672.2010.04914.x.
35. Lin Y, Teng K, Huan L, Zhong J. 2011. Dissection of the bridging pattern of bovicin HJ50, a lantibiotic containing a characteristic disulfide bridge. Microbiol. Res. 166:146-154. http://dx.doi.org/10.1016/j.micres.2010.05.001.
36. Paulsen I, Banerjei L, Myers G, Nelson K, Seshadri R, Read T, Fouts D, Eisen J, Gill S, Heidelberg J. 2003. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299:2071-2074. http://dx.doi.org/10.1126/science.1080613.
37. Islam MR, Nishie M, Nagao J, Zendo T, Keller S, Nakayama J, Kohda D, Sahl HG, Sonomoto K. 2012. Ring A of nukacin ISK-1: a lipid IIbinding motif for type-A (II) lantibiotic. J. Am. Chem. Soc. 134:3687-3690. http://dx.doi.org/10.1021/ja300007h.
38. Epps DE, Wolfe ML, Groppi V. 1994. Characterization of the steadystate and dynamic fluorescence properties of the potential-sensitive dye bis-(1,3-dibutylbarbituric acid) trimethine oxonol (Dibac4(3)) in model systems and cells. Chem. Phys. Lipids 69:137-150. http://dx.doi.org/10.1016/0009-3084(94)90035-3.
39. Li M, Shen X, Yan J, Han H, Zheng B, Liu D, Cheng H, Zhao Y, Rao X, Wang C, Tang J, Hu F, Gao GF. 2011. GI-type T4SS-mediated horizontal transfer of the 89K pathogenicity island in epidemic Streptococcus suis serotype 2. Mol. Microbiol. 79:1670-1683. http://dx.doi.org/10.1111/j.1365-2958.2011.07553.x.
40. Zhang A, Yang M, Hu P, Wu J, Chen B, Hua Y, Yu J, Chen H, Xiao J, Jin M. 2011. Comparative genomic analysis of Streptococcus suis reveals significant genomic diversity among different serotypes. BMC Genomics 12:523. http://dx.doi.org/10.1186/1471-2164-12-523.
41. Shankar N, Coburn P, Pillar C, Haas W, Gilmore M. 2004. Enterococcal cytolysin: activities and association with other virulence traits in a pathogenicity island. Int. J. Med. Microbiol. 293:609-618. http://dx.doi.org/10.1078/1438-4221-00301.
42. Shankar N, Baghdayan AS, Gilmore MS. 2002. Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature 417:746-750. http://dx.doi.org/10.1038/nature00802.
43. Diep DB, Godager L, Brede D, Nes IF. 2006. Data mining and characterization of a novel pediocin-like bacteriocin system from the genome of Pediococcus pentosaceus ATCC 25745. Microbiology 152:1649-1659. http: //dx.doi.org/10.1099/mic.0.28794-0.
44. Shi Y, Yang X, Garg N, van der Donk WA. 2011. Production of lantipeptides in Escherichia coli. J. Am. Chem. Soc. 133:2338-2341. http://dx .doi.org/10.1021/ja109044r.
45. Xiao H, Chen X, Chen M, Tang S, Zhao X, Huan L. 2004. Bovicin HJ50, a novel lantibiotic produced by Streptococcus bovis HJ50. Microbiology 150:103-108. http://dx.doi.org/10.1099/mic.0.26437-0.
46. Georgalaki M, Papadimitriou K, Anastasiou R, Pot B, Van Driessche G, Devreese B, Tsakalidou E. 2013. Macedovicin, the second food-grade lantibiotic produced by Streptococcus macedonicus ACA-DC 198. Food Microbiol. 33:124-130. http://dx.doi.org/10.1016/j.fm.2012.09.008.
47. Shen X, Zhong Q, Zhao Y, Yin S, Chen T, Hu F, Li M. 2013. Proteome analysis of the two-component SalK/SalR system in epidemic Streptococcus suis serotype 2. Curr. Microbiol. 67:118-122. http://dx.doi.org/10.1007/s00284-013-0343-4.
48. Stein T, Borchert S, Kiesau P, Heinzmann S, Klöss S, Klein C, Helfrich M, Entian KD. 2002. Dual control of subtilin biosynthesis and immunity in Bacillus subtilis. Mol. Microbiol. 44:403-416. http://dx.doi.org/10.1046/j.1365-2958.2002.02869.x.