Multi-locus sequence typing and virulence profile in Bacillus cereus sensu lato strains isolated from dairy products

Submitted: 15 July 2019
Accepted: 28 August 2019
Published: 18 January 2021
Abstract Views: 599
PDF: 363
HTML: 10
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

Members of Bacillus cereus group are important food contaminants and they are of relevant interest in food safety and public heath due to their ability to cause two distinct forms of food poisoning, emetic and diarrhoeal syndrome. In the present study, 90 strains of B. cereus isolated from dairy products, have been typed using Multilocus Sequence Typing (MLST) analysis and investigated for the occurrence of 10 enterotoxigenic genes (hblA, hblC, hblD, nheA, nheB, nheC, cytK, entFM, entS and bceT) and one emetogenic gene (ces), to determine their genetic diversity. A total of 58 sequence types were identified and among these 17 were signalled as new profiles. Among the virulence genes, the majority of our strains carried the entS (92%), entFM (86%), nhe (82%) and cytK (72%) genes. All remaining genes were identified in at least one strain with different prevalence, stressing the genetic diversity, how even the different grade of pathogenicity of B. cereus isolated from dairy products.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Agata N, Ohta M, Arakawa Y, Mori M, 1995. The bceT gene of Bacillus cereus encodes an enterotoxic protein. Microbiol 141, 983–988. DOI: https://doi.org/10.1099/13500872-141-4-983
Agata N, Ohta M, Yokoyama K, 2002. Production of Bacillus cereus emetic toxin (cereulide) in various foods. Int J Food Microbiol 73, 23–27. DOI: https://doi.org/10.1016/S0168-1605(01)00692-4
Asano SI, Nukumizu Y, Bando H, Iizuka T, Yamamoto T, 1997. Cloning of novel enterotoxin genes from Bacillus cereus and Bacillus thuringiensis. Appl. Environ. Microbiol 63, 1054–1057. DOI: https://doi.org/10.1128/AEM.63.3.1054-1057.1997
Beecher DJ, Wong AC, 1994. Identification and analysis of the antigens detected by two commercial Bacillus cereus diarrheal enterotoxin immunoassay kits. Appl. Environ. Microbiol 60, 4614–4616. DOI: https://doi.org/10.1128/AEM.60.12.4614-4616.1994
Beuchat LR, Ma-Lin CF, Carpenter JA, 1980. Growth of Bacillus cereus in media containing plant seed materials and ingredients used in Chinese cookery. J Appl Bacteriol 48, 397–407. DOI: https://doi.org/10.1111/j.1365-2672.1980.tb01028.x
Brillard J, Dupont CMS, Berge O, Dargaignaratz C, Oriol-Gagnier S, Doussan C, Broussolle V, Gillon M, Clavel T, Bérard A, 2015. The Water Cycle, a Potential Source of the Bacterial Pathogen Bacillus cereus. Biomed Res Int 2015, 356928. DOI: https://doi.org/10.1155/2015/356928
Cardazzo B, Negrisolo E, Carraro L, Alberghini L, Patarnello T, Giaccone V, 2008. Multiple-locus sequence typing and analysis of toxin genes in Bacillus cereus food-borne isolates. Appl Environ Microbiol 74, 850–860. DOI: https://doi.org/10.1128/AEM.01495-07
Castiaux V, Laloux L, Schneider YJ, Mahillon J, 2016. Screening of Cytotoxic B. cereus on Differentiated Caco-2 Cells and in Co-Culture with Mucus-Secreting (HT29-MTX) Cells. Toxins 5;8(11) DOI: https://doi.org/10.3390/toxins8110320
Chang YH, Shangkuan YH, Lin HC, Liu HW, 2003. PCR Assay of the groEL Gene for Detection and Differentiation of Bacillus cereus Group Cells. Appl Environ Microbiol 69, 4502–4510. DOI: https://doi.org/10.1128/AEM.69.8.4502-4510.2003
Chaves, JQ, Cavados C de FG, Vivoni AM, 2012. Molecular and toxigenic characterization of Bacillus cereus and Bacillus thuringiensis strains isolated from commercial ground roasted coffee. J Food Prot 75, 518–522. DOI: https://doi.org/10.4315/0362-028X.JFP-11-325
Christiansson A, Bertilsson J, Svensson B, 1999. Bacillus cereus spores in raw milk: factors affecting the contamination of milk during the grazing period. J Dairy Sci 82, 305–314. DOI: https://doi.org/10.3168/jds.S0022-0302(99)75237-9
Didelot X, Barker M, Falush D, Priest FG, 2009. Evolution of pathogenicity in the Bacillus cereus group. Syst Appl Microbiol 32, 81–90. DOI: https://doi.org/10.1016/j.syapm.2009.01.001
Ehling-Schulz M, Svensson B, Guinebretiere MH, Lindbäck T, Andersson M, Schulz A, Fricker M, Christiansson A, Granum PE, Märtlbauer E, Nguyen-The C, Salkinoja-Salonen M, Scherer S, 2005. Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains. Microbiol 151, 183–197. DOI: https://doi.org/10.1099/mic.0.27607-0
Fagerlund A, Ween O, Lund T, Hardy SP, Granum PE, 2004. Genetic and functional analysis of the cytK family of genes in Bacillus cereus. Microbiol 150, 2689–2697. DOI: https://doi.org/10.1099/mic.0.26975-0
Fricker M, 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. DOI: https://doi.org/10.1128/AEM.02219-06
Ghelardi E, Celandroni F, Salvetti S, Barsotti C, Baggiani A, Senesi S, 2002. Identification and characterization of toxigenic Bacillus cereus isolates responsible for two food-poisoning outbreaks. FEMS Microbiol Lett 208, 129–134. DOI: https://doi.org/10.1111/j.1574-6968.2002.tb11072.x
Granum PE, Lund T, 1997. Bacillus cereus and its food poisoning toxins. FEMS Microbiol Lett 157, 223–228. DOI: https://doi.org/10.1111/j.1574-6968.1997.tb12776.x
Guinebretière MH, Broussolle V, Nguyen-The C, 2002. Enterotoxigenic profiles of food-poisoning and food-borne Bacillus cereus strains. J Clin Microbiol 40, 3053–3056. DOI: https://doi.org/10.1128/JCM.40.8.3053-3056.2002
Harmon SM, Kautter DA, 1991. Incidence and Growth Potential of Bacillus cereus in Ready-to-Serve Foods. J Food Prot 54, 372–374. DOI: https://doi.org/10.4315/0362-028X-54.5.372
Hendriksen NB, Hansen BM, Johansen JE, 2006. Occurrence and pathogenic potential of Bacillus cereus group bacteria in a sandy loam. Antonie Van Leeuwenhoek 89, 239–249. DOI: https://doi.org/10.1007/s10482-005-9025-y
López AC, Minnaard J, Pérez PF, Alippi AM, 2015. A case of intoxication due to a highly cytotoxic Bacillus cereus strain isolated from cooked chicken. Food Microbiol 46, 195–199. DOI: https://doi.org/10.1016/j.fm.2014.08.005
Madeira JP, Alpha-Bazin B, Armengaud J, Duport C, 2015. Time dynamics of the Bacillus cereus exoproteome are shaped by cellular oxidation. Front Microbiol 6, 342. DOI: https://doi.org/10.3389/fmicb.2015.00342
Owusu-Kwarteng J, Wuni A, Akabanda F, Tano-Debrah K, Jespersen L, 2017. Prevalence, virulence factor genes and antibiotic resistance of Bacillus cereus sensu lato isolated from dairy farms and traditional dairy products. BMC Microbiol 17, 65. DOI: https://doi.org/10.1186/s12866-017-0975-9
Priest FG, Barker M, Baillie LWJ, Holmes EC, Maiden MCJ, 2004. Population structure and evolution of the Bacillus cereus group. J Bacteriol 186, 7959–7970. DOI: https://doi.org/10.1128/JB.186.23.7959-7970.2004
Reis ALS, Montanhini MTM, Bittencourt JVM, Destro MT, Bersot LS, 2013. Gene detection and toxin production evaluation of hemolysin BL of Bacillus cereus isolated from milk and dairy products marketed in Brazil. Braz. J Microbiol 44, 1195–1198. DOI: https://doi.org/10.1590/S1517-83822013000400024
Sergeev N, Distler M, Vargas M, Chizhikov V, Herold KE, Rasooly A, 2006. Microarray analysis of Bacillus cereus group virulence factors. J Microbiol Methods 65, 488–502. DOI: https://doi.org/10.1016/j.mimet.2005.09.013
Wetterhall M, Grönberg A, Grönlund S, Björkman T, Sandberg L, Musunuri S, Chaloupka K, Gammell P, 2019. Removal of B. cereus cereulide toxin from monoclonal antibody bioprocess feed via two-step Protein A affinity and multimodal chromatography. J Chromatogr B Analyt Technol Biomed Life Sci 1118–1119, 194–202. DOI: https://doi.org/10.1016/j.jchromb.2019.04.018
Yang IC, Shih DYC, Huang TP, Huang YP, Wang JY, Pan TM, 2005. Establishment of a novel multiplex PCR assay and detection of toxigenic strains of the species in the Bacillus cereus group. J Food Prot 68, 2123–2130. DOI: https://doi.org/10.4315/0362-028X-68.10.2123
Yang Y, Yu X, Zhan L, Chen J, Zhang Yunyi, Zhang J, Chen H, Zhang Z, Zhang Yanjun, Lu Y, Mei L, 2017. Multilocus sequence type profiles of Bacillus cereus isolates from infant formula in China. Food Microbiol 62, 46–50. DOI: https://doi.org/10.1016/j.fm.2016.09.007
Yim JH, Kim K Y, Chon JW, Kim DH, Kim HS, Choi DS, Choi IS, Seo KH, 2015. Incidence, Antibiotic Susceptibility, and Toxin Profiles of Bacillus cereus sensu lato Isolated from Korean Fermented Soybean Products. J Food Sci 80, M1266-1270. DOI: https://doi.org/10.1111/1750-3841.12872

How to Cite

1.
Bianco A, Capozzi L, Miccolupo A, Iannetti S, Danzetta ML, Del Sambro L, Caruso M, Santagada G, Parisi A. Multi-locus sequence typing and virulence profile in <em>Bacillus cereus sensu</em> lato strains isolated from dairy products. Ital J Food Safety [Internet]. 2021 Jan. 18 [cited 2024 Oct. 8];9(4). Available from: https://www.pagepressjournals.org/ijfs/article/view/8401