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Isolation of Bacillus cereus Group from the Fecal Material of Endangered Wood Turtles

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Abstract

Members of the Bacillus cereus group are opportunistic human pathogens. They can be found in a broad range of foods. Diarrheal food poisoning and/or emetic type syndromes can result from eating contaminated food. In this study, seven B. cereus group members were isolated from the fecal material of Wood Turtles (Glyptemys insculpta). The isolates were then assessed for the presence of enterotoxin genes (nheA, entFM, hblC, and cytK) using PCR. The most prevalent is the nonhemolytic enterotoxin gene which was found in all seven isolates.

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References

  1. Agata N, Mori M, Ohta M, Suwan S, Ohtani I, Isobe M (1994) A novel dodecadepsipeptide, cereulide, isolated from Bacillus cereus vacuole formation in Hep-2 cells. FEMS Microbiol Lett 121:31–34

    CAS  PubMed  Google Scholar 

  2. Agata N, Ohta M, Yokoyama K (2002) Production of Bacillus cereus emetic toxin (cereulide) in various foods. Int J Food Microbiol 73:23–27

    Article  CAS  PubMed  Google Scholar 

  3. Altayar M, Sutherland AD (2006) Bacillus cereus is common in the environment but emetic toxin producing strains are rare. J Appl Microbiol 100:7–14

    Article  CAS  PubMed  Google Scholar 

  4. Andersson A, Rönner U, Granum PE (1995) What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens? Int J Food Microbiol 28:145–155

    Article  CAS  PubMed  Google Scholar 

  5. BarbosaTM Serra CR, La Ragione RM, Woodward MJ, Henriques AO (2005) Screening for Bacillus isolates in the broiler gastrointestinal tract. Appl Environ Microbiol 71:968–978

    Article  Google Scholar 

  6. Bonerba E, Di Pinto A, Novello L, Montemurro F, Terio V, Colao V, Ciccarese G, Tantillo G (2010) Detection of potentially enterotoxigenic food-related Bacillus cereus by PCR analysis. Int J Food Sci Technol 45:1310–1315

    Article  CAS  Google Scholar 

  7. Dierick K, Van Coillie E, Swiecicka I, Meyfroidt G, Devlieger H, Meulemans A, Hoedemaekers G, Fourie L, Heyndrickx M, Mahillon J (2005) Fatal family outbreak of Bacillus cereus associated food poisoning. J Clin Microbiol 43:4277–4279

    Article  PubMed Central  PubMed  Google Scholar 

  8. Ehling-Schulz M, Fricker M, Siegfried S (2004) Identification of emetic toxin producing Bacillus cereus strains by a novel molecular assay. FEMS Mirobiol Lett 232:189–195

    Article  CAS  Google Scholar 

  9. Ehling-Schulz M, Messelhäusser U (2013) Bacillus “next generation” diagnostics: moving from detection toward subtyping and risk-related strain profiling. Front Microbiol 4:1–8

    Article  Google Scholar 

  10. Ernst CH, Zug GR (1994) Observations on the reproductive biology of the spotted turtle, Clemmys guttata, in southeastern Pennsylvania. J Herpetol 28:99–102

    Article  Google Scholar 

  11. Forghani F, Kim JB, Oh DH (2014) Enterotoxigenic profiling of emetic toxin- and enterotoxin-producing Bacillus cereus, isolated from food, environmental, and clinical samples by multiplex PCR. J Food Sci 79:M2288–M2293

    Article  CAS  PubMed  Google Scholar 

  12. FrickerM Messelhäusser U, Busch U, Scherer S, Ehling-Schulz M (2007) Diagnostic real-time PCR assays for the detection of emetic Bacillus cereus strains in foods and recent food-borne outbreaks. Appl Environ Microbiol 73:1892–1898

    Article  Google Scholar 

  13. Grupka LM, Ramsay EC, Bemis DA (2006) Salmonella surveillance in a collection of rattlesnakes (Crotalus spp.). J Zoo Wildl Med 37:306–312

    Article  PubMed  Google Scholar 

  14. Guinebretière MH, Auger S, Galleron N, Contzen M, De Sarrau B, De Buyser ML, Lamberet G, Fagerlund A, Granum PE, Lereclus D, De Vos P, Nguyen-The C, Sorokin A (2013) Bacillus cytotoxicus sp. nov. is a novel thermotolerant species of the Bacillus cereus Group occasionally associated with food poisoning. Int J Syst Evol Microbiol 63:31–40

    Article  PubMed  Google Scholar 

  15. Harding JH, Bloomer TJ (1979) The wood turtle, Clemmys insculpta a natural history. HERP-Bull NY Herpetol Soc 15:9–26

    Google Scholar 

  16. Helgason E, Okstad OA, Caugant DA, Johansen HA, Fouet A, Mock M, Hegna I, Kolstø AB (2000) Bacillus anthracis, Bacillus cereus and Bacillus thuringiensis—one species on the basis genetic evidence. Appl Environ Microbiol 66:2627–2630

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Jensen GB, Hansen BM, Eilenberg J, Mahillon J (2003) The hidden lifestyles of Bacillus cereus and relatives. Environ Microbiol 5:631–640

    Article  CAS  PubMed  Google Scholar 

  18. Jiménez G, Blanch AR, Tamames J, Rosselló-Mora R (2013) Complete genome sequence of Bacillus toyonensis BCT-7112T, the active ingredient of the feed additive preparation Toyocerin. Genome Announc 1:e01013–e01080

    Article  Google Scholar 

  19. Jones TO, Turnbull PC (1981) Bovine mastitis caused by Bacillus cereus. Vet Rec 108:271–274

    Article  CAS  PubMed  Google Scholar 

  20. Kim JB, Kim JM, Kim CH, Seo KS, Park YB, Choi NJ, Oh DH (2010) Emetic toxin producing Bacillus cereus Korean isolates contain genes encoding diarrheal-related enterotoxins. Int J Food Microbiol 144:182–186

    Article  CAS  PubMed  Google Scholar 

  21. Kim JM, Forghani F, Kim JB, Park YB, Park MS, Wang J, Park JH, Oh DH (2012) Improved multiplex PCR assay for simultaneous detection of Bacillus cereus emetic and enterotoxic strains. Food Sci Biotechnol 21:1439–1444

    Article  CAS  Google Scholar 

  22. Marler LM, Siders JA, Wolters LC, Pettigrew Y, Skitt BL, Allen SD (1992) Comparison of five cultural procedures for isolation of Clostridium difficile from stools. J Clin Microbiol 30:514–516

    PubMed Central  CAS  PubMed  Google Scholar 

  23. Martίnez-Blanch JF, Sánchez G, Garay E, Aznar R (2009) Development of a real-time PCR assay for detection and quantification of enterotoxigenic members of Bacillus cereus group in food samples. Int J Food Microbiol 135:15–21

    Article  Google Scholar 

  24. McAuley CM, McMillan K, Moore SC, Fegan N, Fox EM (2014) Prevalence and characterization of foodborne pathogens from Australian dairy farm environments. J Dairy Sci 97:7402–7412

    Article  CAS  PubMed  Google Scholar 

  25. McLaughlin RW, Cochran PA, Dowd SE (2015) Metagenomic analysis of the gut microbiota of the Timber Rattlesnake, Crotalus horridus. Mol Biol Rep 42:1187–1195

    Article  CAS  PubMed  Google Scholar 

  26. Ngamwongsatit P, Buasri W, Pianariyanon P, Pulsrikarn C, Ohba M, Assavanig A, Panbangred W (2008) Broad distribution of enterotoxin genes (hblCDA, nheABC, cytKand entFM) among Bacillus thuringiensis and Bacillus cereus as shown by novel primers. Int J Food Microbiol 121:352–356

    Article  CAS  PubMed  Google Scholar 

  27. Park YB, Kim JB, Shin SW, Kim JC, Cho SH, Lee BK, Ahn J, Kim JM, Oh DH (2009) Prevalence, genetic diversity, and antibiotic susceptibility of Bacillus cereus strains isolated from rice and cereals collected in Korea. J Food Prot 72:612–617

    CAS  PubMed  Google Scholar 

  28. Ross DA, Brewster KN, Anderson RK, Ratner N, Brewster CM (1991) Aspects of the ecology of wood turtles, Clemmys insculpta, in Wisconsin. Can Field-Nat 105:363–367

    Google Scholar 

  29. Sandra A, Afsah-Hejri L, Tunung R, Tuan Zainazor TC, Tang JYH, Ghazali FM, Nakaguchi Y, Nishibuchi M, Son R (2012) Bacillus cereus and Bacillus thuringiensis in ready-to-eat cooked rice in Malaysia. Int Food Res J 19:829–836

    Google Scholar 

  30. Schröter M, Roggentin P, Hofmann J, Speicher A, Laufs R, Mack D (2004) Pet snakes as a reservoir for Salmonella enterica subsp. diarizonae (Serogroup IIIb): a prospective study. Appl Environ Microbiol 70:613–615

    Article  PubMed Central  PubMed  Google Scholar 

  31. vanDijk PP, Harding J (2013) Glyptemys insculpta. The IUCN Red List of Threatened Species. Version 2014.3. www.iucnredlist.org. Downloaded on 07 April 2015

  32. Vilas-Bôas GT, Peruca AP, Arantes OM (2007) Biology and taxonomy of Bacillus cereus, Bacillus anthracis, and Bacillus thuringiensis. Can J Microbiol 53:673–687

    Article  PubMed  Google Scholar 

  33. Wehrle E, Didier A, Moravek M, Dietrich R, Märtlbauer E (2010) Detection of Bacillus cereus with enteropathogenic potential by multiplex real-time PCR based on SYBR Green I. Mol Cell Probes 24:124–130

    Article  CAS  PubMed  Google Scholar 

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Acknowledgment

This research was done as part of a Provost Honors Project under the leadership of Zina Haywood, Executive Vice President/Provost. We also thank Kathy Nordhaus and Donald Zakutansky for their enthusiastic support of this research. This project was supported by funding provided by Gateway Technical College and by the Gateway Foundation.

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Authors and Affiliations

  1. General Studies, Gateway Technical College, Kenosha, WI, 53144, USA

    Nancy Ngvumbo Nfor & Richard William McLaughlin

  2. Wisconsin Department of Natural Resources, Rhinelander, WI, USA

    Carly N. Lapin

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  1. Nancy Ngvumbo Nfor
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  2. Carly N. Lapin
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  3. Richard William McLaughlin
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Correspondence to Richard William McLaughlin.

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Nfor, N.N., Lapin, C.N. & McLaughlin, R.W. Isolation of Bacillus cereus Group from the Fecal Material of Endangered Wood Turtles. Curr Microbiol 71, 524–527 (2015). https://doi.org/10.1007/s00284-015-0875-x

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  • DOI: https://doi.org/10.1007/s00284-015-0875-x

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