Botulinum neurotoxin-encoding plasmids can be conjugatively transferred to diverse clostridial strains

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Nawrocki, Erin M ^a   Bradshaw, Marite ^a   Johnson, Eric A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOTULINUM TOXIN;

ANIMAL; CHROMOSOME; CLOSTRIDIALES; CLOSTRIDIUM; CLOSTRIDIUM BOTULINUM; GENETICS; HUMAN; METABOLISM; MOUSE; PHYLOGENY; PLASMID; TRANSPOSON;

ANIMALS; BOTULINUM TOXINS; CHROMOSOMES; CLOSTRIDIALES; CLOSTRIDIUM; CLOSTRIDIUM BOTULINUM; DNA TRANSPOSABLE ELEMENTS; HUMANS; MICE; PHYLOGENY; PLASMIDS;

EID: 85042197498     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-21342-9     Document Type: Article

References (65)

1. Rossetto, O., Megighian, A., Scorzeto, M. & Montecucco, C. Botulinum neurotoxins. Toxicon 67, 31-36, https://doi. org/10. 1016/j. Toxicon. 2013. 01. 017 (2013).
2. Keesey, J. The most vulnerable synapse: historic aspects of neuromuscular junction disorders. Handb Clin Neurol 91, 1-25, https:// doi. org/10. 1016/s0072-9752(07)01501-1 (2008).
3. Rosow, L. K. & Strober, J. B. Infant botulism: review and clinical update. Pediatr Neurol 52, 487-492, https://doi. org/10. 1016/j. pediatrneurol. 2015. 01. 006 (2015).
4. Smith, T. J., Hill, K. K. & Raphael, B. H. Historical and current perspectives on Clostridium botulinum diversity. Res Microbiol 166, 290-302, https://doi. org/10. 1016/j. resmic. 2014. 09. 007 (2015).
5. Johnson, E. A. & Bradshaw, M. Clostridium botulinum and its neurotoxins: A metabolic and cellular perspective. Toxicon 39, 1703-1722, https://doi. org/10. 1016/S0041-0101(01)00157-X (2001).
6. Connan, C. & Popoff, M. R. Two-component systems and toxinogenesis regulation in Clostridium botulinum. Res Microbiol 166, 332-343, https://doi. org/10. 1016/j. resmic. 2014. 12. 012 (2015).
7. Mansfield, M. J., Adams, J. B. & Doxey, A. C. Botulinum neurotoxin homologs in non-Clostridium species. FEBS Lett 589, 342-348, https://doi. org/10. 1016/j. febslet. 2014. 12. 018 (2015).
8. Zornetta, I. et al. The first non Clostridial botulinum-like toxin cleaves VAMP within the juxtamembrane domain. Sci Rep 6, 30257, https://doi. org/10. 1038/srep30257 (2016).
9. Zhang, S. et al. Identification and characterization of a novel botulinum neurotoxin. Nat Commun 8, 14130, https://doi. org/10. 1038/ ncomms14130 (2017).
10. Carter, A. T. et al. Independent evolution of neurotoxin and flagellar genetic loci in proteolytic Clostridium botulinum. BMC Genomics 10, 115, https://doi. org/10. 1186/1471-2164-10-115 (2009).
11. Carter, A. T. & Peck, M. W. Genomes, neurotoxins and biology of Clostridium botulinum Group I and Group II. Res Microbiol 166, 303-317, https://doi. org/10. 1016/j. resmic. 2014. 10. 010 (2015).
12. Weigand, M. R. et al. Implications of genome-based discrimination between Clostridium botulinum Group I and Clostridium sporogenes strains for bacterial taxonomy. Appl Environ Microbiol 81, 5420-5429, https://doi. org/10. 1128/AEM. 01159-15 (2015).
13. Hill, K. K. et al. 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, https://doi. org/10. 1186/1741-7007-7-66 (2009).
14. Dineen, S. S., Bradshaw, M. & Johnson, E. A. Neurotoxin gene clusters in Clostridium botulinum type A strains: sequence comparison and evolutionary implications. Curr Microbiol 46, 345-352, https://doi. org/10. 1007/s00284-002-3851-1 (2003).
15. Frankel, G., Newton, S. M., Schoolnik, G. K. & Stocker, B. A. Intragenic recombination in a flagellin gene: characterization of the H1-j gene of Salmonella typhi. EMBO J 8, 3149-3152 (1989).
16. Harrington, C. S., Thomson-Carter, F. M. & Carter, P. E. Evidence for recombination in the flagellin locus of Campylobacter jejuni: implications for the flagellin gene typing scheme. J Clin Microbiol 35, 2386-2392 (1997).
17. Smith, N. H., Beltran, P. & Selander, R. K. Recombination of Salmonella phase 1 flagellin genes generates new serovars. J Bacteriol 172, 2209-2216 (1990).
18. Wassenaar, T. M., Fry, B. N. & van der Zeijst, B. A. Variation of the flagellin gene locus of Campylobacter jejuni by recombination and horizontal gene transfer. Microbiology 141(Pt 1), 95-101 (1995).
19. Smith, T. J. et al. 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, e1271, https://doi. org/10. 1371/journal. pone. 0001271 (2007).
20. Weickert, M. J., Chambliss, G. H. & Sugiyama, H. Production of toxin by Clostridium botulinum type A strains cured by plasmids. Appl Environ Microbiol 51, 52-56 (1986).
21. Marshall, K. M., Bradshaw, M., Pellett, S. & Johnson, E. A. Plasmid encoded neurotoxin genes in Clostridium botulinum serotype A subtypes. Biochem Biophys Res Commun 361, 49-54, https://doi. org/10. 1016/j. bbrc. 2007. 06. 166 (2007).
22. Wisniewski, J. A. & Rood, J. I. The Tcp conjugation system of Clostridium perfringens. Plasmid 91, 28-36, https://doi. org/10. 1016/j. plasmid. 2017. 03. 001 (2017).
23. Franciosa, G., Maugliani, A., Scalfaro, C. & Aureli, P. Evidence that plasmid-borne botulinum neurotoxin type B genes are widespread among Clostridium botulinum serotype B strains. PLoS One 4, e4829, https://doi. org/10. 1371/journal. pone. 0004829 (2009).
24. Hosomi, K. 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 289, 1267-1274, https://doi. org/10. 1007/s00438-014-0887-4 (2014).
25. Skarin, H., Hafstrom, T., Westerberg, J. & Segerman, B. Clostridium botulinum group III: A group with dual identity shaped by plasmids, phages and mobile elements. BMC Genomics 12, 185, https://doi. org/10. 1186/1471-2164-12-185 (2011).
26. Zhou, Y., Sugiyama, H., Nakano, H. & Johnson, E. A. The genes for the Clostridium botulinum type G toxin complex are on a plasmid. Infect Immun 63, 2087-2091 (1995).
27. Espelund, M. & Klaveness, D. Botulism outbreaks in natural environments-an update. Front Microbiol 5, 287, https://doi. org/10. 3389/fmicb. 2014. 00287 (2014).
28. Metcalf, J. L. et al. Microbial community assembly and metabolic function during mammalian corpse decomposition. Science 351, 158-162, https://doi. org/10. 1126/science. Aad2646 (2016).
29. von Wintersdorff, C. J. H. et al. Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer. Front Microbiol 7, https://doi. org/10. 3389/fmicb. 2016. 00173 (2016).
30. Montecucco, C. & Rasotto, M. B. On botulinum neurotoxin variability. MBio 6, https://doi. org/10. 1128/mBio. 02131-14 (2015).
31. Collins, M. D. & East, A. K. Phylogeny and taxonomy of the food-borne pathogen Clostridium botulinum and its neurotoxins. J Appl Microbiol 84, 5-17, https://doi. org/10. 1046/j. 1365-2672. 1997. 00313. x (1998).
32. Marshall, K. M., Bradshaw, M. & Johnson, E. A. Conjugative botulinum neurotoxin-encoding plasmids in Clostridium botulinum. PLoS One 5, e11087, https://doi. org/10. 1371/journal. pone. 0011087 (2010).
33. Lin, W. J. & Johnson, E. A. Transposon Tn916 mutagenesis in Clostridium botulinum. Appl Environ Microbiol 57, 2946-2950 (1991).
34. Naglich, J. G. & Andrews, R. E. Jr. Tn916-dependent conjugal transfer of PC194 and PUB110 from Bacillus subtilis into Bacillus thuringiensis subsp. israelensis. Plasmid 20, 113-126 (1988).
35. Showsh, S. A. & Andrews, R. E. Jr. Analysis of the requirement for a pUB110 mob region during Tn916-dependent mobilization. Plasmid 41, 179-186, https://doi. org/10. 1006/plas. 1999. 1398 (1999).
36. Whitmer, M. E. & Johnson, E. A. Development of improved defined media for Clostridium botulinum serotypes A, B, and E. Appl Environ Microbiol 54, 753-759 (1988).
37. Giordani, F. et al. Genomic characterization of Italian Clostridium botulinum group I strains. Infect Genet Evol, 36, 62-71, https://doi. org/10. 1016/j. meegid. 2015. 08. 042 (2015).
38. Skarin, H. & Segerman, B. Plasmidome interchange between Clostridium botulinum, Clostridium novyi and Clostridium haemolyticum converts strains of independent lineages into distinctly different pathogens. PLoS One 9, e107777, https://doi. org/10. 1371/journal. pone. 0107777 (2014).
39. Ng, V. & Lin, W. J. Comparison of assembled Clostridium botulinum A1 genomes revealed their evolutionary relationship. Genomics 103, 94-106, https://doi. org/10. 1016/j. ygeno. 2013. 12. 003 (2014).
40. Dover, N., Barash, J. R., Hill, K. K., Xie, G. & Arnon, S. S. Molecular characterization of a novel botulinum neurotoxin type H gene. J Infect Dis 209, 192-202, https://doi. org/10. 1093/infdis/jit450 (2014).
41. Grohmann, E., Muth, G. & Espinosa, M. Conjugative plasmid transfer in gram-positive bacteria. Microbiol Mol Biol Rev 67, 277-301, https://doi. org/10. 1128/mmbr. 67. 2. 277-301. 2003 (2003).
42. Li, J. et al. Toxin plasmids of Clostridium perfringens. Microbiol Mol Biol Rev 77, 208-233, https://doi. org/10. 1128/mmbr. 00062-12 (2013).
43. Wisniewski, J. A. et al. TcpM: A novel relaxase that mediates transfer of large conjugative plasmids from Clostridium perfringens. Mol Microbiol 99, 884-896, https://doi. org/10. 1111/mmi. 13270 (2016).
44. Adams, V. et al. Virulence plasmids of spore-forming bacteria. Microbiol Spectr 2, https://doi. org/10. 1128/microbiolspec. PLAS-0024-2014 (2014).
45. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J Mol Biol 215, 403-410, https:// doi. org/10. 1016/s0022-2836(05)80360-2 (1990).
46. Lauber, C. L. et al. Vertebrate decomposition is accelerated by soil microbes. Appl Environ Microbiol 80, 4920-4929, https://doi. org/10. 1128/aem. 00957-14 (2014).
47. Metcalf, J. L., Carter, D. O. & Knight, R. Microbiology of death. Curr Biol 26, R561-563, https://doi. org/10. 1016/j. cub. 2016. 03. 042 (2016).
48. Smith, L. & Sugiyama, H. in American Lecture Series in Clinical Microbiology (ed Balows, A.) 2nd edn (Charles C. Thomas, 1988).
49. Bradshaw, M., Tepp, W. H., Whitemarsh, R. C. M., Pellett, S. & Johnson, E. A. Holotoxin activity of botulinum neurotoxin subtype A4 originating from a nontoxigenic Clostridium botulinum expression system. Appl Environ Microbiol 80, https://doi. org/10. 1128/ AEM. 01795-14 (2014).
50. Whitemarsh, R. C., Tepp, W. H., Johnson, E. A. & Pellett, S. Persistence of botulinum neurotoxin A subtypes 1-5 in primary rat spinal cord cells. PLoS One 9, e90252, https://doi. org/10. 1371/journal. pone. 0090252 (2014).
51. Heap, J. T., Pennington, O. J., Cartman, S. T., Carter, G. P. & Minton, N. P. The ClosTron: A universal gene knock-out system for the genus Clostridium. J Microbiol Methods 70, 452-464, https://doi. org/10. 1016/j. mimet. 2007. 05. 021 (2007).
52. Foster, P. L. In vivo mutagenesis. Methods Enzymol 204, 114-125 (1991).
53. Art, Ü. Enhanced butanol production by mutant strains of Clostridium acetobutylicum in molasses medium. Turk J Biochem 33, 25-30 (2008).
54. Johnson, E. A. et al. Characterization of Clostridium botulinum strains associated with an infant botulism case in the United Kingdom. J Clin Microbiol 43, 2602-2607, https://doi. org/10. 1128/jcm. 43. 6. 2602-2607. 2005 (2005).
55. Chomczynski, P. One-hour downward alkaline capillary transfer for blotting of DNA and RNA. Anal Biochem 201, 134-139 (1992).
56. Schantz, E. J. & Kautter, D. Standardized assay for Clostridium botulinum toxins [in foods]. J Assoc Off Anal Chem (1978).
57. Hatheway, C. L. in Laboratory Diagnosis of Infectious Diseases: Principles and Practice (eds Balows, A. et al.) 111-133 (Springer New York, 1988).
58. Maslanka, S. E., Solomon, H. M., Sharma, S. & Johnson, E. A. in Compendium of Methods for the Microbiological Examination of Foods (eds Salfinger, Y. & Tortorello, M. L.) Ch. 32 (American Public Health Association, 2013).
59. Hunter, S. B. et al. Establishment of a universal size standard strain for use with the PulseNet standardized pulsed-field gel electrophoresis protocols: converting the national databases to the new size standard. J Clin Microbiol 43, 1045-1050, https://doi. org/10. 1128/jcm. 43. 3. 1045-1050. 2005 (2005).
60. Schantz, E. J. & Johnson, E. A. Properties and use of botulinum toxin and other microbial neurotoxins in medicine. Microbiol Rev 56, 80-99 (1992).
61. Binz, T. et al. The complete sequence of botulinum neurotoxin type A and comparison with other clostridial neurotoxins. J Biol Chem 265, 9153-9158 (1990).
62. Johnson, E. A., Lin, W. J., Zhou, Y. T. & Bradshaw, M. Characterization of neurotoxin mutants in Clostridium botulinum type A. Clin Infect Dis 25(Suppl 2), S168-170 (1997).
63. Williamson, C. H. et al. Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia. BMC Genomics 17, 180, https://doi. org/10. 1186/s12864-016-2502-z (2016).
64. Schill, K. M. et al. Genetic diversity of Clostridium sporogenes PA 3679 isolates obtained from different sources as resolved by pulsedfield gel electrophoresis and high-throughput sequencing. Appl Environ Microbiol 82, 384-393, https://doi. org/10. 1128/aem. 02616-15 (2015).
65. Wang, X. et al. Genetic analysis of type E botulinum toxin-producing Clostridium butyricum strains. Appl Environ Microbiol 66, 4992-4997, https://doi. org/10. 1128/aem. 66. 11. 4992-4997. 2000 (2000).