Plasmid characterization and chromosome analysis of two netf+ clostridium perfringens isolates associated with foal and canine necrotizing enteritis

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Gohari, Iman Mehdizadeh ^a   Kropinski, Andrew M ^a   Weese, Scott J ^a   Parreira, Valeria R ^a   Whitehead, Ashley E ^b   Boerlin, Patrick ^a   Prescott, John F ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOCIN; CLOSTRIDIUM TOXIN; CPB2 TOXIN; CPE TOXIN; NETE TOXIN; NETF TOXIN; UNCLASSIFIED DRUG; BACTERIAL TOXIN;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENOME; BACTERIAL STRAIN; CLOSTRIDIUM PERFRINGENS; DOG; FOAL; GASTROENTERITIS; GENE SEQUENCE; HAEMORRHAGIC GASTROENTERITIS; NECROTIZING ENTERITIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY ISLAND; PLASMID; ANIMAL; CHROMOSOME; CLOSTRIDIUM INFECTION; ENTERITIS; GENE LOCUS; GENETICS; GENOMICS; HORSE; MICROBIOLOGY; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; VETERINARY;

ANIMALS; BACTERIAL TOXINS; CHROMOSOMES; CLOSTRIDIUM INFECTIONS; CLOSTRIDIUM PERFRINGENS; DOGS; ENTERITIS; GENETIC LOCI; GENOMICS; HORSES; PLASMIDS; SEQUENCE ANALYSIS; SPECIES SPECIFICITY;

EID: 84959441525     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0148344     Document Type: Article

References (56)

1. Songer JG. Clostridial enteric diseases of domestic animals. Clin Microbiol Rev. 1996; 9:216-234. PMID: 8964036.
2. McClane BA, Uzal FA, Miyakawa MF, Lyerly D, Wilkins TD. The enterotoxic clostridia. In: Dworkin M, Falkow S, Rosenburg E, Schleifer H, Stackebrandt E, editors. The prokaryotes: a handbook on the biology of bacteria. Springer; 2006. pp. 688-752.
3. Hatheway C. Toxigenic clostridia. Clin Microbiol Rev. 1990; 3:66-76. PMID: 2404569.
4. Petit L, Gilbert M, Popoff M. Clostridium perfringens: Toxinotype and genotype. Trends Microbiol. 1999; 7:104-110. PMID: 10203838.
5. Uzal FA, Vidal JE, McClane BA, Gurjar AA. Clostridium Perfringens toxins involved in mammalian veterinary diseases. Open Toxinology J. 2010; 2:24-42. PMID: 24511335.
6. Mehdizadeh Gohari I, Parreira VR, Nowell VJ, Nicholson VM, Oliphant K, Prescott JF. A novel poreforming toxin in type A Clostridium perfringens is associated with both fatal canine hemorrhagic gastroenteritis and fatal foal necrotizing enterocolitis. PLoS One. 2015 Apr 8; 10(4):e0122684. doi:10.1371/journal.pone.0122684 PMID: 25853427.
7. Shimizu TK, Ohtani H, Hirakawa K, Ohshima A, Yamashita T, Shiba N, et al. Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc Natl Acad Sci. 2002; 99:996- 1001. PMID: 11792842.
8. Myers GS, Rasko DA, Cheung JK, Ravel J, Seshadri R, DeBoy RT, et al. Skewed genomic variability in strains of the toxigenic bacterial pathogen, Clostridium perfringens. Genome Res. 2006; 16:1031- 1040. PMID: 16825665.
9. Parreira VR, Costa M, Eikmeyer F, Blom J, Prescott JF. Sequence of two plasmids from Clostridium perfringens chicken necrotic enteritis isolates and comparison with C. perfringens conjugative plasmids. PLoS One. 2012 Nov 26; 7(11): e49753. doi:10.1371/journal.pone.0049753 PMID: 23189158.
10. Hassan KA, Elbourne LD, Tetu SG, Melville SB, Rood JI, Paulsen IT. Genome analyses of Clostridium perfringens isolates from five toxinotypes. Res Microbiol. 2015; 166:255-263doi:10.1016/j.resmic.2014.10.003PMID: 25445567.
11. Lepp D, Roxas B, Parreira VR, Marri PR, Rosey EL, Gong J, et al. Identification of novel pathogenicity loci in Clostridium perfringens strains that cause avian necrotic enteritis. PLoS One. 2010 May 24; 5 (5): e10795. doi:10.1371/journal.pone.0010795 PMID: 20532244.
12. Li J, Adams V, Bannam TL, Miyamoto K, Garcia JP, Uzal FA, et al. Toxin plasmids of Clostridium perfringens. Microbiol Mol Biol Rev. 2013; 77:208-233. doi:10.1128/MMBR.00062-12PMID: 23699255.
13. Yonogi S, Matsuda S, Kawai T, Yoda T, Harada T, Kumeda Y, et al. BEC, a novel enterotoxin of Clostridium perfringens found in human clinical isolates from acute gastroenteritis outbreaks. Infect Immun. 2014; 82:2390-2399doi:10.1128/IAI.01759-14 PMID: 24664508.
14. Brynestad S, Sarker MR, McClane BA, Granum PE, Rood JI. Enterotoxin plasmid from Clostridium perfringens is conjugative. Infect Immun. 2001; 69:3483-3487. PMID: 11292780.
15. Hughes ML, Poon R, Adams V, Sayeed S, Saputo J, Uzal FA, et al. Epsilon-toxin plasmids of Clostridium perfringens type D are conjugative. J Bacteriol. 2007; 189:7531-7538. PMID: 17720791.
16. Bannam TL, Yan XX, Harrison PE, Seemann T, Keyburn AL, Stubenrauch C, et al. Necrotic enteritisderived Clostridium perfringens strain with three closely related independently conjugative toxin and antibiotic resistance plasmids. MBio. 2011 Sep 27; 2(5): e00190-11doi:10.1128/mBio.00190-11 PMID: 21954306.
17. Rood JI, Scott VN, Duncan CL. Identification of a transferable tetracycline resistance plasmid (pCW3) from Clostridium perfringens. Plasmid. 1978; 1:563-570. PMID: 219433.
18. Abraham LJ, Wales AJ, Rood JI. Worldwide distribution of the conjugative Clostridium perfringens tetracycline resistance plasmid, pCW3. Plasmid. 1985; 14:37-46. PMID: 2863833.
19. Bannam TL, Teng WL, Bulach D, Lyras D, Rood JI. Functional identification of conjugation and replication regions of the tetracycline resistance plasmid pCW3 from Clostridium perfringens. J Bacteriol. 2006; 188:4942-4951. PMID: 16788202.
20. Bantwal R, Bannam TL, Porter CJ, Quinsey NS, Lyras D, Adams V, et al. The peptidoglycan hydrolase TcpG is required for efficient conjugative transfer of pCW3 in Clostridium perfringens. Plasmid. 2012; 67:139-147. doi:10.1016/j.plasmid.2011.12.016 PMID: 22244927.
21. Porter CJ, Banwal R, Bannam TL, Rosado CJ, Pearce MC, Adams V, et al. The conjugation protein TcpC from Clostridium perfringens is structurally related to the type IV secretion system protein VirB8 from Gram-negative bacteria. Mol Microbiol. 2012; 83:275-288. doi:10.1111/j.1365-2958.2011.07930.x PMID: 22150951.
22. Miyamoto K, Li J, Sayeed S, Akimoto S, McClane BA. Sequencing and diversity analyses reveal extensive similarities between some epsilon-toxin-encoding plasmids and the pCPF5603 Clostridium perfringens enterotoxin plasmid. J Bacteriol. 2008; 190:7178-7188. doi:10.1128/JB.00939-08 PMID: 18776010.
23. Pospiech A, Neumann B. A versatile quick-prep of genomic DNA from Gram-positive bacteria. Trends Genet. 1995; 11:217-218. PMID: 7638902.
24. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One. 2010 Jun 25; 5(6): e11147doi:10.1371/journal.pone.0011147PMID: 20593022.
25. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 2014 Jan 1; 42: D206-D214. doi:10.1093/nar/gkt1226 PMID: 24293654.
26. Altschul S, Warren G, Webb M, Eugene M, Lipman D. Basic local alignment search tool. J Mol Biol. 1990; 215:403-410. PMID: 2231712.
27. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: a fast phage search tool. Nucleic Acids Res. 2011 Jul 1; 7(39):W347-52. doi:10.1093/nar/gkr485.
28. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics. 2011 Apr 1; 27(7): 1009-1010. doi:10.1093/bioinformatics/btr039PMID: 21278367.
29. Ohtani K, Hirakawa H, Tashiro K, Yoshizawa S, Kuhara S, Shimizu T. Identification of a two-component VirR/VirS regulon in Clostridium perfringens. Anaerobe. 2010; 16:258-264doi:10.1016/j.anaerobe.2009.10.003 PMID: 19835966.
30. Cheung JK, Keyburn AL, Carter GP, Lanckriet AL, Van Immerseel F, Moore RJ, et al. The VirSR twocomponent signal transduction system regulates NetB toxin production in Clostridium perfringens. Infect Immun. 2010; 78:3064-3072. doi:10.1128/IAI.00123-10 PMID: 20457789.
31. Cheung JK, Dupuy B, Deveson DS, Rood JI. The spatial organization of the VirR boxes is critical for VirR-mediated expression of the perfringolysin O gene, pfoA, from Clostridium perfringens. J Bacteriol. 2004; 186:3321-3330. PMID: 15150217.
32. Stothard P, Wishart DS. Circular genome visualization and exploration using CGView. Bioinformatics. 2005; 21:537-539. PMID: 15479716.
33. McClane BA. An overview of Clostridium perfringens enterotoxin. Toxicon.1996; 34:1335-1343. PMID: 9027990.
34. Sparks SG, Carman RJ, Sarker MR, McClane BA. Genotyping of enterotoxigenic Clostridium perfringens fecal isolates associated with antibiotic-associated diarrhea and food poisoning in North America. J Clin Microbiol. 2001; 39:883-888. PMID: 11230399.
35. Keyburn AL, Boyce JD, Vaz P, Bannam TL, Ford ME, Parker D, et al. NetB, a new toxin that is associated with avian necrotic enteritis caused by Clostridium perfringens. PLoS Pathog. 2008 Feb 8; 4(2): e26. doi:10.1371/journal.ppat.0040026 PMID: 18266469.
36. Chalmers G, Bruce HL, Hunter DB, Parreira VR, Kulkarni RR, Jiang YF, et al. Multilocus sequence typing analysis of Clostridium perfringens isolates from necrotic enteritis outbreaks in broiler chicken populations. J Clin Microbiol. 2008; 46:3957-3964. doi:10.1128/JCM.01548-08 PMID: 18945840.
37. Uzal FA, Freedman JC, Shrestha A, Theoret JR, Garcia J, Awad MM, et al. Towards an understanding of the role of Clostridium perfringens toxins in human and animal disease. Future Microbiol. 2014; 9:361-377doi:10.2217/fmb.13.168 PMID: 24762309.
38. Tagg JR, Dajani AS, Wannamaker LW. Bacteriocins of Gram-positive bacteria. Microbiol Mol Biol Rev. 1976; 40:722-756.
39. Barbara AJ, Trinh HT, Glock RD, Songer GJ. Necrotic enteritis-producing strains of Clostridium perfringens displace non-necrotic enteritis strains from the gut of chicks. Vet Microbiol. 2008; 126:377-82. PMID: 17850994 40.
40. Lacobino A, Scalfaro C, Franciosa G. Structure and genetic content of the megaplasmids of neurotoxigenic Clostridium butyricum type E strains from Italy. PLoS One. 2013 Aug 15; 8(8):e71324. doi:10.1371/journal.pone.0071324 PMID: 23967192.
41. Hosomi K, Sakaguchi Y, Kohda T, Gotoh K, Motooka D, Nakamura S, et al. Complete nucleotide sequence of a plasmid containing the botulinum neurotoxin gene in Clostridium botulinum type B strain 111 isolated from an infant patient in Japan. Mol Genet Genomics. 2014; 289:1267-1274. doi:10.1007/s00438-014-0887-4 PMID: 25149145.
42. Hamon M, Bierne H, Cossart P. Listeria monocytogenes: a multifaceted model. Nat Rev Micro. 2006; 4:423-434.
43. Bruggemann H, Bauumer S, Fricke WF, Wiezer A, Liesegang H, Decker I, et al. The genome sequence of Clostridium tetani, the causative agent of tetanus disease. Proc Natl Acad Sci USA. 2003; 100:1316-1321. PMID: 12552129.
44. Sebaihia M, Peck MW, Minton NP, Thomson NR, Holden MT, Mitchell WJ, et al. Genome sequence of a proteolytic (Group I) Clostridium botulinum strain Hall A and comparative analysis of the clostridial genomes. Genome Res. 2007; 17:1082-1092. PMID: 17519437.
45. Bella J, Hindle KL, McEwan PA, Lovell SC. The leucine-rich repeat structure. Cell Mol Life Sci. 2008; 65:2307-2333. doi:10.1007/s00018-008-8019-0 PMID: 18408889.
46. Deivanayagam CC, Rich RL, Carson M, Owens RT, Danthuluri S, Bice T, et al. Novel fold and assembly of the repetitive B region of the Staphylococcus aureus collagen-binding surface protein. Structure. 2000; 8:67-78. PMID: 10673425.
47. Spraggon G, Koesema E, Scarselli M, Malito E, Biagini M, Norais N, et al. Supramolecular organization of the repetitive backbone unit of the Streptococcus pneumonia pilus. PLoS One. 2010 Jun 15; 5(6): e10919. doi:10.1371/journal.pone.0010919 PMID: 20559564.
48. Miyamoto K, Chakrabarti G, Morino Y, McClane BA. Organization of the plasmid cpe locus of Clostridium perfringens type A isolates. Infect Immun. 2002; 70:4261-4272. PMID: 12117935.
49. Miyamoto K, Fisher DJ, Li J, Sayeed S, Akimoto S, McClane BA, et al. Complete sequencing and diversity analysis of the enterotoxin-encoding plasmids in Clostridium perfringens type A non-food-borne human gastrointestinal disease isolates. J Bacteriol. 2006; 188:1585-1598. PMID: 16452442.
50. Li J, Miyamoto K, Sayeed S, McClane BA. Organization of the cpe Locus in CPE-Positive Clostridium perfringens Type C and D Isolates. PLoS One. 2010 Jun 3; 5(6): e10932. doi:10.1371/journal.pone.0010932 PMID: 20532170.
51. Govind R, Dupuy B. Secretion of Clostridium difficile toxins A and B requires the holing-like protein TcdE. PLoS Pathog. 2012 Jun 7; 8(6):e1002727. doi:10.1371/journal.ppat.1002727 PMID: 22685398.
52. Nakiang S, Ndeh DA, Wipat A, Bolam DN, Hirt RP. A novel extracellular metallopeptidase domain shared by animal host-associated mutualistic and pathogenic microbes. PLoS One. 2012 Jan 27; 7(1): e30287. doi:10.1371/journal.pone.0030287PMID: 22299034.
53. Gaskell A, Crennell S, Tavlor G. The three domains of a bacterial sialidase: a beta-propeller, an immunoglobulin module and a galactose-binding jelly-roll. Structure. 1995; 3:1197-1205. PMID: 8591030.
54. Cornillot E, Saint-Joanis B, Daube G, Katayama S, Granum PE, Canard B, et al. The enterotoxin gene (cpe) of Clostridium perfringens can be chromosomal or plasmid-borne. Mol Microbiol. 1995; 15:639- 647. PMID: 7783636.
55. Lindstrom M, Heikinheimo A, Lahti P, Korkeala H. Novel insights into the epidemiology of Clostridium perfringens type A food poisoning. Food Microbiol. 2011; 28:192-198. doi:10.1016/j.fm.2010.03.020 PMID: 21315973.
56. Nowell VJ, Kropinski AM, Songer JG, MacInnes JI, Perreira VR, Prescott JF. Genome sequencing and analysis of a type A Clostridium perfringens isolate from a case of bovine clostridial abomasitis. PLoS One. 2012 Mar 8; 7(3):e32271. doi:10.1371/journal.pone.0032271 PMID: 22412860.