Functional analysis of a bacitracin resistance determinant located on ICECp1, a novel tn916-like element from a conjugative plasmid in clostridium perfringens

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 11, 2015, Pages 6855-6865

  Han, Xiaoyan ^a   Du, Xiang Dang ^a,b   Southey, Luke ^a   Bulach, Dieter M ^a   Seemann, Torsten ^a   Yan, Xu Xia ^a   Bannam, Trudi L ^a   Rood, Julian I ^a  

^a MONASH UNIVERSITY   (Australia)

^b HENAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACITRACIN; BACTERIAL TOXIN; NETB TOXIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; BIRD; CLOSTRIDIUM PERFRINGENS; ENTEROCOCCUS FAECALIS; GENE LOCUS; GENETIC PARAMETERS; INTEGRATIVE CONJUGATIVE ELEMENTS P1; MUTAGENESIS; NECROTIZING ENTERITIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; REGULATOR GENE; STRUCTURAL GENE; WILD TYPE; BACTERIAL GENE; BACTERIUM CONJUGATION; DRUG EFFECTS; GENETICS;

ANTI-BACTERIAL AGENTS; BACITRACIN; CLOSTRIDIUM PERFRINGENS; CONJUGATION, GENETIC; GENES, BACTERIAL; PLASMIDS;

EID: 84946203775     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01643-15     Document Type: Article

References (45)

1. Keyburn AL, Boyce JD, Vaz P, Bannam TL, Ford ME, Parker D, Di Rubbo A, Rood JI, Moore RJ. 2008. NetB, a new toxin that is associated with avian necrotic enteritis caused by Clostridium perfringens. PLoS Pathog 4:e26. http://dx.doi.org/10.1371/journal.ppat.0040026.
2. Brennan J, Skinner J, Barnum DA, Wilson J. 2003. The efficacy of bacitracin methylene disalicylate when fed in combination with narasin in the management of necrotic enteritis in broiler chickens. Poult Sci 82: 360-363. http://dx.doi.org/10.1093/ps/82.3.360.
3. Prescott JF, Sivendra R, Barnum DA. 1978. The use of bacitracin in the prevention and treatment of experimentally-induced necrotic enteritis in the chicken. Can Vet J 19:181-183.
4. Phillips I. 2007. Withdrawal of growth-promoting antibiotics in Europe and its effects in relation to human health. Int J Antimicrob Agents 30: 101-107. http://dx.doi.org/10.1016/j.ijantimicag.2007.02.018.
5. Charlebois A, Jalbert LA, Harel J, Masson L, Archambault M. 2012. Characterization of genes encoding for acquired bacitracin resistance in Clostridium perfringens. PLoS One 7:e44449. http://dx.doi.org/10.1371/journal.pone.0044449.
6. Lepp D, Roxas B, Parreira VR, Marri PR, Rosey EL, Gong J, Songer JG, Vedantam G, Prescott JF. 2010. Identification of novel pathogenicity loci in Clostridium perfringens strains that cause avian necrotic enteritis. PLoS One 5:e10795. http://dx.doi.org/10.1371/journal.pone.0010795.
7. Mascher T, Margulis NG, Wang T, Ye RW, Helmann JD. 2003. Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon. Mol Microbiol 50:1591-1604. http://dx.doi.org/10.1046/j.1365-2958.2003.03786.x.
8. Storm DR, Strominger JL. 1973. Complex formation between bacitracin peptides and isoprenyl pyrophosphates. The specificity of lipid-peptide interactions. J Biol Chem 248:3940-3945.
9. Manson JM, Keis S, Smith JM, Cook GM. 2004. Acquired bacitracin resistance in Enterococcus faecalis is mediated by an ABC transporter and a novel regulatory protein, BcrR. Antimicrob Agents Chemother 48:3743-3748. http://dx.doi.org/10.1128/AAC.48.10.3743-3748.2004.
10. 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. http://dx.doi.org/10.1111/j.1365-2958.1995.tb02322.x.
11. Ohki R, Giyanto Tateno K, Masuyama W, Moriya S, Kobayashi K, Ogasawara N. 2003. The BceRS two-component regulatory system induces expression of the bacitracin transporter, BceAB, in Bacillus subtilis. Mol Microbiol 49:1135-1144. http://dx.doi.org/10.1046/j.1365-2958.2003.03653.x.
12. Tsuda H, Yamashita Y, Shibata Y, Nakano Y, Koga T. 2002. Genes involved in bacitracin resistance in Streptococcus mutans. Antimicrob Agents Chemother 46:3756-3764. http://dx.doi.org/10.1128/AAC.46.12.3756-3764.2002.
13. Gebhard S, Gaballa A, Helmann JD, Cook GM. 2009. Direct stimulus perception and transcription activation by a membrane-bound DNA binding protein. Mol Microbiol 73:482-491. http://dx.doi.org/10.1111/j.1365-2958.2009.06787.x.
14. Wang XM, Li XS, Wang YB, Wei FS, Zhang SM, Shang YH, Du XD. 2015. Characterization of a multidrug resistance plasmid from Enterococcus faecium that harbours a mobilized bcrABDR locus. J Antimicrob Chemother 70:609-611. http://dx.doi.org/10.1093/jac/dku416.
15. Cain BD, Norton PJ, Eubanks W, Nick HS, Allen CM. 1993. Amplification of the bacA gene confers bacitracin resistance to Escherichia coli. J Bacteriol 175:3784-3789.
16. Chalker AF, Ingraham KA, Lunsford RD, Bryant AP, Bryant J, Wallis NG, Broskey JP, Pearson SC, Holmes DJ. 2000. The bacA gene, which determines bacitracin susceptibility in Streptococcus pneumoniae and Staphylococcus aureus, is also required for virulence. Microbiology 146: 1547-1553.
17. Bernard R, Joseph P, Guiseppi A, Chippaux M, Denizot F. 2003. YtsCD and YwoA, two independent systems that confer bacitracin resistance to Bacillus subtilis. FEMS Microbiol Lett 228:93-97. http://dx.doi.org/10.1016/S0378-1097(03)00738-9.
18. Pollock TJ, Thorne L, Yamazaki M, Mikolajczak MJ, Armentrout RW. 1994. Mechanism of bacitracin resistance in gram-negative bacteria that synthesize exopolysaccharides. J Bacteriol 176:6229-6237.
19. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Rood JI, Maher EA, Somers EB, Campos E, Duncan CL. 1978. Isolation and characterization of multiply antibiotic-resistant Clostridium perfringens strains from porcine feces. Antimicrob Agents Chemother 13:871-880. http://dx.doi.org/10.1128/AAC.13.5.871.
21. Rood JI. 1983. Transferable tetracycline resistance in Clostridium perfringensstrainsofporcine origin. CanJMicrobiol 29:1241-1246. http://dx.doi.org/10.1139/m83-193.
22. Inoue H, Nojima H, Okayama H. 1990. High efficiency transformation of Escherichia coli with plasmids. Gene 96:23-28. http://dx.doi.org/10.1016/0378-1119(90)90336-P.
23. Scott PT, Rood JI. 1989. Electroporation-mediated transformation of lysostaphin-treated Clostridium perfringens. Gene 82:327-333. http://dx.doi.org/10.1016/0378-1119(89)90059-0.
24. O'Connor JR, Lyras D, Farrow KA, Adams V, Powell DR, Hinds J, Cheung JK, Rood JI. 2006. Construction and analysis of chromosomal Clostridium difficile mutants. Mol Microbiol 61:1335-1351. http://dx.doi.org/10.1111/j.1365-2958.2006.05315.x.
25. Han X, Kennan RM, Parker D, Davies JK, Rood JI. 2007. Type IV fimbrial biogenesis is required for protease secretion and natural transformation in Dichelobacter nodosus. J Bacteriol 189:5022-5033. http://dx.doi.org/10.1128/JB.00138-07.
26. Bannam TL, Yan XX, Harrison PF, Seemann T, Keyburn AL, Stubenrauch C, Weeramantri LH, Cheung JK, McClane BA, Boyce JD, Moore RJ, Rood JI. 2011. Necrotic enteritis-derived Clostridium perfringens strain with three closely related independently conjugative toxin and antibiotic resistance plasmids. mBio 2(5):e00190-11. http://dx.doi.org/10.1128/mBio.00190-11.
27. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821-829. http://dx.doi.org/10.1101/gr.074492.107.
28. Cheung JK, Keyburn AL, Carter GP, Lanckriet AL, Van Immerseel F, Moore RJ, Rood JI. 2010. The VirSR two-component signal transduction system regulates NetB toxin production in Clostridium perfringens. Infect Immun 78:3064-3072. http://dx.doi.org/10.1128/IAI.00123-10.
29. Adams V, Bantwal R, Stevenson L, Cheung JK, Awad MM, Nicholson J, Carter GP, Mackin KE, Rood JI, Lyras D. 2014. Utility of the clostridial site-specific recombinase TnpX to clone toxic-product-encoding genes and selectively remove genomic DNA fragments. Appl Environ Microbiol 80:3597-3603. http://dx.doi.org/10.1128/AEM.04285-13.
30. Rood JI, Scott VN, Duncan CL. 1978. Identification of a transferable resistance plasmid (pCW3) from Clostridium perfringens. Plasmid 1:563-570. http://dx.doi.org/10.1016/0147-619X(78)90013-6.
31. Li J, Adams V, Bannam TL, Miyamoto K, Garcia JP, Uzal FA, Rood JI, McClane BA. 2013. Toxin plasmids of Clostridium perfringens. Microbiol Mol Biol Rev 77:208-233. http://dx.doi.org/10.1128/MMBR.00062-12.
32. Bannam TL, Teng WL, Bulach D, Lyras D, Rood JI. 2006. Functional identification of conjugation and replication regions of the tetracycline resistance plasmid pCW3 from Clostridium perfringens. J Bacteriol 188: 4942-4951. http://dx.doi.org/10.1128/JB.00298-06.
33. Porter CJ, Bantwal R, Bannam TL, Rosado CJ, Pearce MC, Adams V, Lyras D, Whisstock JC, Rood JI. 2012. The conjugation protein TcpC from Clostridium perfringens is structurally related to the type IV secretion system protein VirB8 from Gram-negative bacteria. Mol Microbiol 83: 275-288. http://dx.doi.org/10.1111/j.1365-2958.2011.07930.x.
34. Gebhard S, Fang C, Shaaly A, Leslie DJ, Weimar MR, Kalamorz F, Carne A, Cook GM. 2014. Identification and characterization of a bacitracin resistance network in Enterococcus faecalis. Antimicrob Agents Chemother 58:1425-1433. http://dx.doi.org/10.1128/AAC.02111-13.
35. Matos R, Pinto VV, Ruivo M, Lopes MDFS. 2009. Study on the dissemination of the bcrABDR cluster in Enterococcus spp. reveals that the BcrAB transporter is sufficient to confer high-level bacitracin resistance. Int J Antimicrob Agents 34:142-147. http://dx.doi.org/10.1016/j.ijantimicag.2009.02.008.
36. Franke AE, Clewell DB. 1981. Evidence for a chromosome-borne resistance transposon (Tn916) in Streptococcus faecalis that is capable of "conjugal" transfer in the absence of a conjugal plasmid. J Bacteriol 145:494-502.
37. Roberts AP, Mullany P. 2011. Tn916-like genetic elements: a diverse group of modular mobile elements conferring antibiotic resistance. FEMS Microbiol Rev 35:856-871. http://dx.doi.org/10.1111/j.1574-6976.2011.00283.x.
38. Su YA, He P, Clewell DB. 1992. Characterization of the tet(M) determinant of Tn916: evidence for regulation by transcription attenuation. Antimicrob Agents Chemother 36:769-778. http://dx.doi.org/10.1128/AAC.36.4.769.
39. Roberts AP, Johanesen PA, Lyras D, Mullany P, Rood JI. 2001. Comparison of Tn5397 from Clostridium difficile, Tn916 from Enterococcus faecalisand the CW459tet(M) element from Clostridium perfringens shows that they have similar conjugation regions but different insertion and excision modules. Microbiology 147:1243-1251.
40. Rice LB, Carias LL, Marshall SH, Hutton-Thomas R, Rudin S. 2007. Characterization of Tn5386, a Tn916-related mobile element. Plasmid 58: 61-67. http://dx.doi.org/10.1016/j.plasmid.2007.01.002.
41. Soge OO, Beck NK, White TM, No DB, Roberts MC. 2008. A novel transposon, Tn6009, composed of a Tn916 element linked with a Staphylococcus aureus mer operon. J Antimicrob Chemother 62:674-680. http://dx.doi.org/10.1093/jac/dkn255.
42. Nowell VJ, Kropinski AM, Songer JG, MacInnes JI, Parreira VR, Prescott JF. 2012. Genome sequencing and analysis of a type A Clostridium perfringens isolate from a case of bovine clostridial abomasitis. PLoS One 7:e32271. http://dx.doi.org/10.1371/journal.pone.0032271.
43. de Vries LE, Christensen H, Skov RL, Aarestrup FM, Agerso Y. 2009. Diversity of the tetracycline resistance gene tet(M) and identification of Tn916- and Tn5801-like (Tn6014) transposons in Staphylococcus aureus from humans and animals. J Antimicrob Chemother 64:490-500. http://dx.doi.org/10.1093/jac/dkp214.
44. Keyburn AL, Sheedy SA, Ford ME, Williamson MM, Awad MM, Rood JI, Moore RJ. 2006. Alpha-toxin of Clostridium perfringens is not an essential virulence factor in necrotic enteritis in chickens. Infect Immun 74:6496-6500. http://dx.doi.org/10.1128/IAI.00806-06.
45. Lyristis M, Bryant AE, Sloan J, Awad MM, Nisbet IT, Stevens DL, Rood JI. 1994. Identification and molecular analysis of a locus that regulates extracellular toxin production in Clostridium perfringens. Mol Microbiol 12:761-777. http://dx.doi.org/10.1111/j.1365-2958.1994.tb01063.x.