SmbFT, a putative ABC transporter complex, confers protection against the lantibiotic smb in streptococci

Journal of Bacteriology

Volumn 195, Issue 24, 2013, Pages 5592-5601

  Biswas, Saswati ^a   Biswas, Indranil ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BACITRACIN; BACTERIAL PROTEIN; BACTERIOCIN; ERYTHROMYCIN; HALODURACIN; LANTIBIOTIC; MUTACIN IV; NISIN; OLIGONUCLEOTIDE; POLYMYXIN B; POLYPEPTIDE ANTIBIOTIC AGENT; SMBF PROTEIN; SMBT PROTEIN; UNCLASSIFIED DRUG; VANCOMYCIN;

AMINO ACID SEQUENCE; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL IMMUNITY; BINDING SITE; CONTROLLED STUDY; CROSS PROTECTION; DELETION MUTANT; ESCHERICHIA COLI; GENE DELETION; GENE INACTIVATION; HETEROLOGOUS EXPRESSION; MOUTH FLORA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STREPTOCOCCUS GALLOLYTICUS; STREPTOCOCCUS MUTANS;

ATP-BINDING CASSETTE TRANSPORTERS; BACTERIOCINS; DRUG RESISTANCE, BACTERIAL; GENE DELETION; GENE EXPRESSION; STREPTOCOCCUS MUTANS; SUBSTRATE SPECIFICITY;

EID: 84890175413     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01060-13     Document Type: Article

References (66)

1. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE. 2005. Defining the normal bacterial flora of the oral cavity. J. Clin. Microbiol. 43:5721-5732.
2. Norder Grusell E, Dahlen G, Ruth M, Ny L, Quiding-Jarbrink M, Bergquist H, Bove M. 2013. Bacterial flora of the human oral cavity, and the upper and lower esophagus. Dis. Esophagus 26:84-90.
3. Que YA, Moreillon P. 2011. Infective endocarditis. Nat. Rev. Cardiology 8:322-336.
4. Nakano K, Ooshima T. 2009. Serotype classification of Streptococcus mutans and its detection outside the oral cavity. Future Microbiol. 4:891-902.
5. Mitchell J. 2011. Streptococcus mitis: walking the line between commensalism and pathogenesis. Mol. Oral Microbiol. 26:89-98.
6. Doern CD, Burnham CA. 2010. It's not easy being green: the viridans group streptococci, with a focus on pediatric clinical manifestations. J. Clin. Microbiol. 48:3829-3835.
7. Burton JP, Wescombe PA, Cadieux PA, Tagg JR. 2011. Beneficial microbes for the oral cavity: time to harness the oral streptococci? Beneficial Microbes 2:93-101.
8. Kreth J, Merritt J, Shi W, Qi F. 2005. Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J. Bacteriol. 187:7193-7203.
9. Qi F, Kreth J. 2010. Characterization of anti-competitor activities produced by oral bacteria. Methods Mol. Biol. 666:151-166.
10. Kreth J, Zhang Y, Herzberg MC. 2008. Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J. Bacteriol. 190:4632-4640.
11. van Belkum MJ, Stiles ME. 2000. Nonlantibiotic antibacterial peptides from lactic acid bacteria. Natural Product Rep. 17:323-335.
12. 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.
13. Willey JM, van der Donk WA. 2007. Lantibiotics: peptides of diverse structure and function. Annu. Rev. Microbiol. 61:477-501.
14. Chatterjee C, Paul M, Xie L, van der Donk WA. 2005. Biosynthesis and mode of action of lantibiotics. Chemical Rev. 105:633-684.
15. Diep DB, Nes IF. 2002. Ribosomally synthesized antibacterial peptides in Gram positive bacteria. Curr. Drug Targets 3:107-122.
16. Woodyer RD, Li G, Zhao H, van der Donk WA. 2007. New insight into the mechanism of methyl transfer during the biosynthesis of fosfomycin. Chem. Commun. 4:359-361.
17. Knerr PJ, van der Donk WA. 2012. Discovery, biosynthesis, and engineering of lantipeptides. Annu. Rev. Biochem. 81:479-505.
18. McClerren AL, Cooper LE, Quan C, Thomas PM, Kelleher NL, van der Donk WA. 2006. Discovery and in vitro biosynthesis of haloduracin, a two-component lantibiotic. Proc. Natl. Acad. Sci. U.S.A. 103:17243-17248.
19. McAuliffe O, Hill C, Ross RP. 2000. Each peptide of the two-component lantibiotic lacticin 3147 requires a separate modification enzyme for activity. Microbiology 146(Pt 9):2147-2154.
20. Kodani S, Lodato MA, Durrant MC, Picart F, Willey JM. 2005. SapT, a lanthionine-containing peptide involved in aerial hyphae formation in the streptomycetes. Mol. Microbiol. 58:1368-1380.
21. Tillotson RD, Wosten HA, Richter M, Willey JM. 1998. A surface active protein involved in aerial hyphae formation in the filamentous fungus Schizophyllum commune restores the capacity of a bald mutant of the filamentous bacterium Streptomyces coelicolor to erect aerial structures. Mol. Microbiol. 30:595-602.
22. Bierbaum G, Sahl HG. 2009. Lantibiotics: mode of action, biosynthesis, and bioengineering. Curr. Pharm. Biotechnol. 10:2-18.
23. Cotter PD, Hill C, Ross RP. 2005. Bacteriocins: developing innate immunity for food. Nat. Rev. Microbiol. 3:777-788.
24. Cotter PD, Hill C, Ross RP. 2005. Bacterial lantibiotics: strategies to improve therapeutic potential. Curr. Protein Peptide Sci. 6:61-75.
25. Heng CK WP, Burton JP, Jack RW, Tagg JR. 2007. The diversity of bacteriocins in Gram-positive bacteria, p 45-92. In Riley MA (ed), Bacteriocins: ecology and evolution. Springer-Verlag, Berlin, Germany.
26. Draper LA, Ross RP, Hill C, Cotter PD. 2008. Lantibiotic immunity. Curr. Protein Peptide Sci. 9:39-49.
27. Hoffmann A, Schneider T, Pag U, Sahl HG. 2004. Localization and functional analysis of PepI, the immunity peptide of Pep5-producing Staphylococcus epidermidis strain 5. Appl. Environ. Microbiol. 70:3263-3271.
28. Stein T, Heinzmann S, Dusterhus S, Borchert S, Entian KD. 2005. Expression and functional analysis of the subtilin immunity genes spaIFEG in the subtilin-sensitive host Bacillus subtilis MO1099. J. Bacteriol. 187:822-828.
29. Stein T, Heinzmann S, Solovieva I, Entian KD. 2003. Function of Lactococcus lactis nisin immunity genes nisI and nisFEG after coordinated expression in the surrogate host Bacillus subtilis. J. Biol. Chem. 278:89-94.
30. Hillman JD, Novak J, Sagura E, Gutierrez JA, Brooks TA, Crowley PJ, Hess M, Azizi A, Leung K, Cvitkovitch D, Bleiweis AS. 1998. Genetic and biochemical analysis of mutacin 1140, a lantibiotic from Streptococcus mutans. Infect. Immun. 66:2743-2749.
31. Qi F, Chen P, Caufield PW. 1999. Purification of mutacin III from group III Streptococcus mutans UA787 and genetic analyses of mutacin III biosynthesis genes. Appl. Environ. Microbiol. 65:3880-3887.
32. Qi F, Chen P, Caufield PW. 1999. Functional analyses of the promoters in the lantibiotic mutacin II biosynthetic locus in Streptococcus mutans. Appl. Environ. Microbiol. 65:652-658.
33. Qi F, Chen P, Caufield PW. 2000. Purification and biochemical characterization of mutacin I from the group I strain of Streptococcus mutans, CH43, and genetic analysis of mutacin I biosynthesis genes. Appl. Environ. Microbiol. 66:3221-3229.
34. Tsang P, Merritt J, Nguyen T, Shi W, Qi F. 2005. Identification of genes associated with mutacin I production in Streptococcus mutans using random insertional mutagenesis. Microbiology 151:3947-3955.
35. Yonezawa H, Kuramitsu HK. 2005. Genetic analysis of a unique bacteriocin, Smb, produced by Streptococcus mutans GS5. Antimicrob. Agents Chemother. 49:541-548.
36. Mota-Meira M, Lacroix C, LaPointe G, Lavoie MC. 1997. Purification and structure of mutacin B-Ny266: a new lantibiotic produced by Streptococcus mutans. FEBS Lett. 410:275-279.
37. Robson CL, Wescombe PA, Klesse NA, Tagg JR. 2007. Isolation and partial characterization of the Streptococcus mutans type AII lantibiotic mutacin K8. Microbiology 153:1631-1641.
38. de Vos WM, Kuipers OP, van der Meer JR, Siezen RJ. 1995. Maturation pathway of nisin and other lantibiotics: posttranslationally modified antimicrobial peptides exported by gram-positive bacteria. Mol. Microbiol. 17:427-437.
39. Sahl HG, Bierbaum G. 1998. Lantibiotics: biosynthesis and biological activities of uniquely modified peptides from gram-positive bacteria. Annu. Rev. Microbiol. 52:41-79.
40. Nicolas GG, Lavoie MC, LaPointe G. 2007. Molecular genetics, genomics and biochemistry of mutacins, vol 1. Global Science Books, London, United Kingdom.
41. Kamiya RU, Hofling JF, Goncalves RB. 2008. Frequency and expression of mutacin biosynthesis genes in isolates of Streptococcus mutans with different mutacin-producing phenotypes. J. Med. Microbiol. 57:626-635.
42. Ajdic D, McShan WM, McLaughlin RE, Savic G, Chang J, Carson MB, Primeaux C, Tian R, Kenton S, Jia H, Lin S, Qian Y, Li S, Zhu H, Najar F, Lai H, White J, Roe BA, Ferretti JJ. 2002. Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc. Natl. Acad. Sci. U.S.A. 99:14434-14439.
43. Biswas S, Biswas I. 2012. Complete genome sequence of Streptococcus mutans GS-5, a serotype c strain. J. Bacteriol. 194:4787-4788.
44. Matsumoto-Nakano M, Kuramitsu HK. 2006. Role of bacteriocin immunity proteins in the antimicrobial sensitivity of Streptococcus mutans. J. Bacteriol. 188:8095-8102.
45. Biswas I, Drake L, Johnson S, Thielen D. 2007. Unmarked gene modification in Streptococcus mutans by a cotransformation strategy with a thermosensitive plasmid. Biotechniques 42:487-490.
46. Biswas I, Jha JK, Fromm N. 2008. Shuttle expression plasmids for genetic studies in Streptococcus mutans. Microbiology 154:2275-2282.
47. Hossain MS, Biswas I. 2012. An extracellular protease, SepM, generates functional competence-stimulating peptide in Streptococcus mutans UA159. J. Bacteriol. 194:5886-5896.
48. Maguin E, Prevost H, Ehrlich SD, Gruss A. 1996. Efficient insertional mutagenesis in lactococci and other gram-positive bacteria. J. Bacteriol. 178:931-935.
49. Banas JA, Biswas S, Zhu M. 2011. Effects of DNA methylation on expression of virulence genes in Streptococcus mutans. Appl. Environ. Microbiol. 77:7236-7242.
50. Petersen FC, Fimland G, Scheie AA. 2006. Purification and functional studies of a potent modified quorum-sensing peptide and a two-peptide bacteriocin in Streptococcus mutans. Mol. Microbiol. 61:1322-1334.
51. Facklam R. 2002. What happened to the streptococci: overview of taxonomic and nomenclature changes. Clin. Microbiol. Rev. 15:613-630.
52. Okuda K, Yanagihara S, Sugayama T, Zendo T, Nakayama J, Sonomoto K. 2010. Functional significance of the E loop, a novel motif conserved in the lantibiotic immunity ATP-binding cassette transport systems. J. Bacteriol. 192:2801-2808.
53. Aas JA, Griffen AL, Dardis SR, Lee AM, Olsen I, Dewhirst FE, Leys EJ, Paster BJ. 2008. Bacteria of dental caries in primary and permanent teeth in children and young adults. J. Clin. Microbiol. 46:1407-1417.
54. Xu P, Ge X, Chen L, Wang X, Dou Y, Xu JZ, Patel JR, Stone V, Trinh M, Evans K, Kitten T, Bonchev D, Buck GA. 2011. Genome-wide essential gene identification in Streptococcus sanguinis. Sci. Rep. 1:125.
55. Aso Y, Okuda K, Nagao J, Kanemasa Y, Thi Bich Phuong N, Koga H, Shioya K, Sashihara T, Nakayama J, Sonomoto K. 2005. A novel type of immunity protein, NukH, for the lantibiotic nukacin ISK-1 produced by Staphylococcus warneri ISK-1. Biosci. Biotechnol. Biochem. 69:1403-1410.
56. Hinse D, Vollmer T, Ruckert C, Blom J, Kalinowski J, Knabbe C, Dreier J. 2011. Complete genome and comparative analysis of Streptococcus gallolyticus subsp. gallolyticus, an emerging pathogen of infective endocarditis. BMC Genomics 12:400. doi:10.1186/1471-2164-12-400.
57. Dintner S, Staron A, Berchtold E, Petri T, Mascher T, Gebhard S. 2011. Coevolution of ABC transporters and two-component regulatory systems as resistance modules against antimicrobial peptides in Firmicutes Bacteria. J. Bacteriol. 193:3851-3862.
58. Gebhard S. 2012. ABC transporters of antimicrobial peptides in Firmicutes bacteria: phylogeny, function, and regulation. Mol. Microbiol. 86:1295-1317.
59. Podlesek Z, Comino A, Herzog-Velikonja B, Zgur-Bertok D, Komel R, Grabnar M. 1995. Bacillus licheniformis bacitracin-resistance ABC transporter: relationship to mammalian multidrug resistance. Mol. Microbiol. 16:969-976.
60. Butcher BG, Lin YP, Helmann JD. 2007. The yydFGHIJ operon of Bacillus subtilis encodes a peptide that induces the LiaRS two-component system. J. Bacteriol. 189:8616-8625.
61. Neumuller AM, Konz D, Marahiel MA. 2001. The two-component regulatory system BacRS is associated with bacitracin 'self-resistance' of Bacillus licheniformis ATCC 10716. Eur. J. Biochem. 268:3180-3189.
62. Davidson AL, Chen J. 2004. ATP-binding cassette transporters in bacteria. Annu. Rev. Biochem. 73:241-268.
63. Draper LA, Grainger K, Deegan LH, Cotter PD, Hill C, Ross RP. 2009. Cross-immunity and immune mimicry as mechanisms of resistance to the lantibiotic lacticin 3147. Mol. Microbiol. 71:1043-1054.
64. Valsesia G, Medaglia G, Held M, Minas W, Panke S. 2007. Circumventing the effect of product toxicity: development of a novel two-stage production process for the lantibiotic gallidermin. Appl. Environ. Microbiol. 73:1635-1645.
65. Puramattathu TV, Islam MR, Nishie M, Yanagihara S, Nagao J, Okuda K, Zendo T, Nakayama J, Sonomoto K. 2012. Enhanced production of nukacin D13E in Lactococcus lactis NZ9000 by the additional expression of immunity genes. Appl. Microbiol. Biotechnol. 93:671-678.
66. Cooper LE, McClerren AL, Chary A, van der Donk WA. 2008. Structure-activity relationship studies of the two-component lantibiotic haloduracin. Chem. Biol. 15:1035-1045.