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

Springer Science and Business Media LLC - Tập 289 - Trang 1267-1274 - 2014
Koji Hosomi1, Yoshihiko Sakaguchi2, Tomoko Kohda1, Kazuyoshi Gotoh3, Daisuke Motooka3, Shota Nakamura3, Kaoru Umeda4, Tetsuya Iida3, Shunji Kozaki1, Masafumi Mukamoto1
1Department of Veterinary Science, Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Izumisano, Japan
2Interdisciplinary Research Organization, University of Miyazaki, Miyazaki, Japan
3Department of Infection Metagenomics, Research Institute for Microbial Diseases, Osaka University, Suita, Japan
4Department of Microbiology, Osaka City Institute of Public Health and Environmental Sciences, Osaka, Japan

Tóm tắt

Botulinum neurotoxins (BoNTs) are highly potent toxins that are produced by Clostridium botulinum. We determined the complete nucleotide sequence of a plasmid containing the botulinum neurotoxin gene in C. botulinum type B strain 111 in order to obtain an insight into the toxigenicity and evolution of the bont gene in C. botulinum. Group I C. botulinum type B strain 111 was isolated from the first case of infant botulism in Japan in 1995. In previous studies, botulinum neurotoxin subtype B2 (BoNT/B2) produced by strain 111 exhibited different antigenic properties from those of authentic BoNT/B1 produced by strain Okra. We have recently shown that the isolates of strain 111 that lost toxigenicity were cured of the plasmid containing the bont/B2 gene. In the present study, the plasmid (named pCB111) was circular 265,575 bp double-stranded DNA and contained 332 predicted open reading frames (ORFs). 85 gene products of these ORFs could be functionally assigned on the basis of sequence homology to known proteins. The bont/B2 complex genes were located on pCB111 and some gene products may be involved in the conjugative plasmid transfer and horizontal transfer of bont genes. pCB111 was similar to previously identified plasmids containing bont/B1, /B5, or/A3 complex genes in other group I C. botulinum strains. It was suggested that these plasmids had been derived from a common ancestor and had played important roles for the bont gene transfer between C. botulinum.

Tài liệu tham khảo

Alouf JE, Freer JH (1999) The comprehensive sourcebook of bacterial protein toxins. In: Popoff MR, Marvaud JC (eds) Structural and genomic features of clostridial neurotoxins, 2nd edn. Academic Press, San Diego, pp 174–201 Arnon SS, Schechter R, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, Fine AD, Hauer J, Layton M, Lillibridge S, Osterholm MT, O’Toole T, Parker G, Perl TM, Russell PK, Swerdlow DL, Tonat K (2001) Botulinum toxin as a biological weapon: medical and public health management. J Am Med Assoc 285(8):1059–1070 Barash JR, Arnon SS (2013) A novel strain of Clostridium botulinum that produces type B and type H botulinum toxins. J Infect Dis 209(2):183–191. doi:10.1093/infdis/jit449 Cornet F, Mortier I, Patte J, Louarn JM (1994) Plasmid pSC101 harbors a recombination site, psi, which is able to resolve plasmid multimers and to substitute for the analogous chromosomal Escherichia coli site dif. J Bacteriol 176(11):3188–3195 Das B, Martinez E, Midonet C, Barre FX (2013) Integrative mobile elements exploiting Xer recombination. Trends Microbiol 21(1):23–30. doi:10.1016/j.tim.2012.10.003 Dover N, Barash JR, Hill KK, Xie G, Arnon SS (2013) Molecular characterization of a novel botulinum neurotoxin type h gene. J Infect Dis 209(2):192–202. doi:10.1093/infdis/jit450 Edmond BJ, Guerra FA, Blake J, Hempler S (1977) Case of infant botulism in Texas. Tex Med 73(10):85–88 Efron B, Halloran E, Holmes S (1996) Bootstrap confidence levels for phylogenetic trees. Proc Natl Acad Sci USA 93(23):13429–13434 Eklund MW, Poysky FT, Reed SM, Smith CA (1971) Bacteriophage and the toxigenicity of Clostridium botulinum type C. Science 172(3982):480–482 Fox CK, Keet CA, Strober JB (2005) Recent advances in infant botulism. Pediatr Neurol 32(3):149–154 Fujinaga Y, Matsumura T, Jin Y, Takegahara Y, Sugawara Y (2009) A novel function of botulinum toxin-associated proteins: HA proteins disrupt intestinal epithelial barrier to increase toxin absorption. Toxicon 54(5):583–586. doi:10.1016/j.toxicon.2008.11.014 Hatheway CL (1990) Toxigenic clostridia. Clin Microbiol Rev 3(1):66–98 Hielm S, Bjorkroth J, Hyytia E, Korkeala H (1998) Genomic analysis of Clostridium botulinum group II by pulsed-field gel electrophoresis. Appl Environ Microbiol 64(2):703–708 Hill KK, Smith TJ (2013) Genetic diversity within clostridium botulinum serotypes, botulinum neurotoxin gene clusters and toxin subtypes. Curr Top Microbiol Immunol 364:1–20. doi:10.1007/978-3-642-33570-9_1 Hill KK, Xie G, Foley BT, Smith TJ, Munk AC, Bruce D, Smith LA, Brettin TS, Detter JC (2009) Recombination and insertion events involving the botulinum neurotoxin complex genes in Clostridium botulinum types A, B, E and F and Clostridium butyricum type E strains. BMC Biol 7:66. doi:10.1186/1741-7007-7-66 Huber KE, Waldor MK (2002) Filamentous phage integration requires the host recombinases XerC and XerD. Nature 417(6889):656–659 Ihara H, Kohda T, Morimoto F, Tsukamoto K, Karasawa T, Nakamura S, Mukamoto M, Kozaki S (2003) Sequence of the gene for Clostridium botulinum type B neurotoxin associated with infant botulism, expression of the C-terminal half of heavy chain and its binding activity. Biochim Biophys Acta 1625(1):19–26 Kakinuma H, Maruyama H, Takahashi H, Yamakawa K, Nakamura S (1996) The first case of type B infant botulism in Japan. Acta Paediatr Jpn 38(5):541–543 Kohda T, Ihara H, Seto Y, Tsutsuki H, Mukamoto M, Kozaki S (2007) Differential contribution of the residues in C-terminal half of the heavy chain of botulinum neurotoxin type B to its binding to the ganglioside GT1b and the synaptotagmin 2/GT1b complex. Microb Pathog 42(2–3):72–79 Kozaki S, Kamata Y, Nishiki T, Kakinuma H, Maruyama H, Takahashi H, Karasawa T, Yamakawa K, Nakamura S (1998) Characterization of Clostridium botulinum type B neurotoxin associated with infant botulism in japan. Infect Immun 66(10):4811–4816 Lamanna C, Glassman HN (1947) The isolation of type B Botulinum Toxin. J Bacteriol 54(5):575–584 Mahillon J, Chandler M (1998) Insertion sequences. Microbiol Mol Biol Rev 62(3):725–774 Matsumura T, Jin Y, Kabumoto Y, Takegahara Y, Oguma K, Lencer WI, Fujinaga Y (2008) The HA proteins of botulinum toxin disrupt intestinal epithelial intercellular junctions to increase toxin absorption. Cell Microbiol 10(2):355–364 Montecucco C, Schiavo G (1995) Structure and function of tetanus and botulinum neurotoxins. Q Rev Biophys 28(4):423–472 Nakayama K, Takashima K, Ishihara H, Shinomiya T, Kageyama M, Kanaya S, Ohnishi M, Murata T, Mori H, Hayashi T (2000) The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage. Mol Microbiol 38(2):213–231 Ohtsubo Y, Ikeda-Ohtsubo W, Nagata Y, Tsuda M (2008) GenomeMatcher: a graphical user interface for DNA sequence comparison. BMC Bioinform 9:376. doi:10.1186/1471-2105-9-376 Peck MW (2009) Biology and genomic analysis of Clostridium botulinum. Adv Microb Physi 55(183–265):320. doi:10.1016/S0065-2911(09)05503-9 Raffestin S, Marvaud JC, Cerrato R, Dupuy B, Popoff MR (2004) Organization and regulation of the neurotoxin genes in Clostridium botulinum and Clostridium tetani. Anaerobe 10(2):93–100 Sakaguchi Y, Hayashi T, Kurokawa K, Nakayama K, Oshima K, Fujinaga Y, Ohnishi M, Ohtsubo E, Hattori M, Oguma K (2005) The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny. Proc Natl Acad Sci USA 102(48):17472–17477 Sebaihia M, Peck MW, Minton NP, Thomson NR, Holden MT, Mitchell WJ, Carter AT, Bentley SD, Mason DR, Crossman L, Paul CJ, Ivens A, Wells-Bennik MH, Davis IJ, Cerdeno-Tarraga AM, Churcher C, Quail MA, Chillingworth T, Feltwell T, Fraser A, Goodhead I, Hance Z, Jagels K, Larke N, Maddison M, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Sanders M, Simmonds M, White B, Whithead S, Parkhill J (2007) Genome sequence of a proteolytic (group I) Clostridium botulinum strain Hall A and comparative analysis of the clostridial genomes. Genome Res 17(7):1082–1092 Smith TJ, Hill KK, Foley BT, Detter JC, Munk AC, Bruce DC, Doggett NA, Smith LA, Marks JD, Xie G, Brettin TS (2007) Analysis of the neurotoxin complex genes in Clostridium botulinum A1-A4 and B1 strains: BoNT/A3, /Ba4 and/B1 clusters are located within plasmids. PLoS One 2(12):e1271 Sugiyama H (1980) Clostridium botulinum neurotoxin. Microbiol Rev 44(3):419–448 Umeda K, Seto Y, Kohda T, Mukamoto M, Kozaki S (2009) Genetic characterization of Clostridium botulinum associated with type B infant botulism in Japan. J Clin Microbiol 47(9):2720–2728. doi:10.1128/JCM.00077-09 Umeda K, Seto Y, Kohda T, Mukamoto M, Kozaki S (2012) Stability of toxigenicity in proteolytic Clostridium botulinum type B upon serial passage. Microbiol Immunol 56(5):338–341. doi:10.1111/j.1348-0421.2012.00441.x Umeda K, Wada T, Kohda T, Kozaki S (2013) Multi-locus variable number tandem repeat analysis for Clostridium botulinum type B isolates in Japan: comparison with other isolates and genotyping methods. Infect Genet Evol 16:298–304. doi:10.1016/j.meegid.2013.02.022 Yamaichi Y, Niki H (2000) Active segregation by the Bacillus subtilis partitioning system in Escherichia coli. Proc Natl Acad Sci USA 97(26):14656–14661 Yamakawa K, Karasawa T, Kakinuma H, Maruyama H, Takahashi H, Nakamura S (1997) Emergence of Clostridium botulinum type B-like nontoxigenic organisms in a patient with type B infant botulism. J Clin Microbiol 35(8):2163–2164 Ye Q, Roh Y, Carroll SL, Blair B, Zhou J, Zhang CL, Fields MW (2004) Alkaline anaerobic respiration: isolation and characterization of a novel alkaliphilic and metal-reducing bacterium. Appl Environ Microbiol 70(9):5595–5602. doi:10.1128/AEM.70.9.5595-5602.2004 Zielenkiewicz U, Ceglowski P (2001) Mechanisms of plasmid stable maintenance with special focus on plasmid addiction systems. Acta Biochim Pol 48(4):1003–1023