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Prevalence and Genetic Diversity of Bacillus cereus Isolated from Raw Milk and Cattle Farm Environments

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Abstract

Bacillus cereus not only has adverse effects on the nutrition and shelf life of dairy products but also seriously endanger people’s health. This study was conducted to reveal the prevalence and genetic diversity of B. cereus strains isolated from raw milk and cattle farm environments. A total 56 of B. cereus strains were detected from 300 environmental samples (soil, water, fodder, air, milk pails, milking machines, cowsheds, bedding, excrement, cow surfaces, udders, overalls, soles, and staff hand samples) and 50 raw milk samples, and divided into 18 sequence types (STs) using multilocus sequence typing method. These STs included ST27, ST61, ST92, ST142, ST168, ST208, ST378, ST427, ST766, ST 857, ST1098, ST1140, ST1194, ST1236, ST1336, ST1339, ST1341, and ST1348, among them, ST857 (7/56, 12.5%) was the dominant ST, and were detected from air, cowsheds, bedding, excrement, and raw milk samples. Our findings could reveal the distribution and genetic diversity of B. cereus strains in raw milk and cattle farm environments, and provide a theoretical basis for controlling the potential harm of this pathogenic bacteria in dairy products.

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References

  1. Ankolekar C, Rahmati T, Labbé RG (2009) Detection of toxigenic Bacillus cereus and Bacillus thuringiensis spores in U.S. rice. Int J Food Microbiol 128(3):460–466. https://doi.org/10.1016/j.ijfoodmicro.2008.10.006

    Article  CAS  PubMed  Google Scholar 

  2. Bartoszewicz M, Hansen BM, Swiecicka I (2008) The members of the Bacillus cereus group are commonly present contaminants of fresh and heat-treated milk. Food Microbiol 25(4):588–596. https://doi.org/10.1016/j.fm.2008.02.001

    Article  CAS  PubMed  Google Scholar 

  3. Bavykin SG, Lysov YP, Zakhariev V, Kelly JJ, Jackman J, Stahl DA, Cherni A (2004) Use of 16S rRNA, 23S rRNA, and gyrB gene sequence analysis to determine phylogenetic relationships of Bacillus cereus group microorganisms. J Clin Microbiol 42(8):3711–3730. https://doi.org/10.1128/JCM.42.8.3711-3730.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Chaves JQ, de Paiva EP, Rabinovitch L, Vivoni AM (2017) Molecular characterization and risk assessment of Bacillus cereus sensu lato isolated from ultrahigh-temperature and pasteurized milk marketed in Rio de Janeiro. Brazil. J Food Protect 80(7):1060–1065. https://doi.org/10.4315/0362-028X.JFP-16-448

    Article  CAS  Google Scholar 

  5. Chen ML, Tsen HY (2010) Discrimination of Bacillus cereus and Bacillus thuringiensis with 16S rRNA and gyrB gene based PCR primers and sequencing of their annealing sites. J Appl Microbiol 92(5):912–919. https://doi.org/10.4315/0362-028X.JFP-16-448

    Article  Google Scholar 

  6. Ehling-Schulz M, Frenzel E, Gohar M (2015) Food–bacteria interplay: pathometabolism of emetic Bacillus cereus. Front Microbiol 6:704. https://doi.org/10.3389/fmicb.2015.00704

    Article  PubMed  PubMed Central  Google Scholar 

  7. Fei P, Jiang Y, Gong S, Li R, Jiang Y, Yuan X, Wang Z, Kang H, Ali MA (2018) Occurrence, genotyping, and antibiotic susceptibility of Cronobacter spp. in drinking water and food samples from Northeast China. J Food Protect 81(3):456–460. https://doi.org/10.4315/0362-028x.jfp-17-326

    Article  CAS  Google Scholar 

  8. Fei P, Jiang Y, Jiang Y, Yuan X, Yang T, Chen J, Wang Z, Kang H, Forsythe SJ (2017) Prevalence, molecular characterization, and antibiotic susceptibility of Cronobacter sakazakii isolates from powdered infant formula collected from Chinese retail markets. Front Microbiol 8:2026. https://doi.org/10.3389/fmicb.2017.02026

    Article  PubMed  PubMed Central  Google Scholar 

  9. Fei P, Man C, Lou B, Forsythe SJ, Chai Y, Li R, Niu J, Jiang Y (2015) Genotyping and source tracking of Cronobacter sakazakii and C malonaticus isolates from powdered infant formula and an infant formula production factory in China. Appl Environ Microb 81(16):5430–5439. https://doi.org/10.1128/aem.01390-15

    Article  CAS  Google Scholar 

  10. Fei P, Xu Y, Zhao S, Gong S, Guo G (2019) Olive oil polyphenols extract inhibits vegetative cells of Bacillus cereus isolated from raw milk. J Dairy Sci 102(5):3894–3902. https://doi.org/10.3168/jds.2018-15184

    Article  CAS  PubMed  Google Scholar 

  11. Fossi BT, Nchanji GT, Wanji S (2017) Occurrence, heat and antibiotic resistance profile of Bacillus cereus isolated from raw cow and processed milk in Mezam Division, Cameroon. Int J Dairy Technol 70(1):43–51. https://doi.org/10.1111/1471-0307.12315

    Article  CAS  Google Scholar 

  12. Gao T, Ding Y, Wu Q, Wang J, Zhang J, Yu S, Yu P, Liu C, Kong L, Feng Z (2018) Prevalence, virulence genes, antimicrobial susceptibility, and genetic diversity of Bacillus cereus isolated from pasteurized milk in China. Front Microbiol 9:533. https://doi.org/10.3389/fmicb.2018.00533

    Article  PubMed  PubMed Central  Google Scholar 

  13. Kumari S, Sarkar PK (2014) Prevalence and characterization of Bacillus cereus group from various marketed dairy products in India. Dairy Sci Technol 94(5):483–497. https://doi.org/10.1007/s13594-014-0174-5

    Article  Google Scholar 

  14. Kumari S, Sarkar PK (2016) Bacillus cereus hazard and control in industrial dairy processing environment. Food Control 69:20–29. https://doi.org/10.1016/j.foodcont.2016.04.012

    Article  Google Scholar 

  15. Lin Y, Ren F, Zhao L, Guo H (2017) Genotypes and the persistence survival phenotypes of Bacillus cereus isolated from UHT milk processing lines. Food Control 82:48–56. https://doi.org/10.1016/j.foodcont.2017.06.025

    Article  CAS  Google Scholar 

  16. Malek F, Boudjemaa BM, Aouar-Métri A, Kihal M (2013) Identification and genetic diversity of Bacillus cereus strains isolated from a pasteurized milk processing line in Algeria. Dairy Sci Technol 93(1):73–82. https://doi.org/10.1007/s13594-012-0093-2

    Article  Google Scholar 

  17. Merzougui S, Lkhider M, Grosset N, Gautier M, Cohen N (2014) Prevalence, PFGE typing, and antibiotic resistance of Bacillus cereus group isolated from food in Morocco. Foodborne Pathog Dis 11(2):145–149. https://doi.org/10.1089/fpd.2013.1615

    Article  CAS  PubMed  Google Scholar 

  18. Ministry of Health of the People’s Republic of China (2010) GB4789.40-2010. National Food Safety Standard: Food Microbiological Examination: Bacillus cereus[S]. China Standard Press, Beijing

    Google Scholar 

  19. Mugadza DT, Owusu-Darko R, Buys EM (2019) Short communication: source tracking Bacillus cereus in an extended-shelf-life milk processing plant using partial sequencing of rpoB and multilocus sequence typing. J Dairy Sci 102(1):135–139. https://doi.org/10.3168/jds.2018-14733

    Article  CAS  PubMed  Google Scholar 

  20. NěMečková I, Pechačová M, Roubal P (2009) Problems with detection of proteolytic microorganisms and their undesirable activities in milk. Czech J Food Sci 27(2):82–89. https://doi.org/10.17221/666-CJFS

    Article  Google Scholar 

  21. Parihar HS (2014) Bacillus cereus. Encyclopedia of. Toxicology 70(12):353–354. https://doi.org/10.1016/B978-0-12-386454-3.00997-0

    Article  Google Scholar 

  22. Reis AL, Montanhini MT, Bittencourt JV, 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(4):1195–1198. https://doi.org/10.1590/S1517-83822013000400024

    Article  PubMed  Google Scholar 

  23. Schoeni JL, Wong AC (2005) Bacillus cereus food poisoning and its toxins. J Food Protect 68(3):636–648. https://doi.org/10.4315/0362-028X-68.3.636

    Article  CAS  Google Scholar 

  24. Shaheen R, Svensson B, Andersson MA, Christiansson A, Salkinoja-Salonen M (2010) Persistence strategies of Bacillus cereus spores isolated from dairy silo tanks. Food Microbiol 27(3):347–355. https://doi.org/10.1016/j.fm.2009.11.004

    Article  CAS  PubMed  Google Scholar 

  25. Van OI, Bagamboula CF, Vanmuysen SC, Wuytack EY, Michiels CW (2004) Inactivation of Bacillus cereus spores in milk by mild pressure and heat treatments. Int J Food Microbiol 92(2):227–234. https://doi.org/10.1016/j.ijfoodmicro.2003.09.011

    Article  Google Scholar 

  26. Yang Y, Yu X, Zhan L, Chen J, Zhang Y, Zhang J, Chen H, Zhang Z, Zhang Y, Lu Y (2017) Multilocus sequence type profiles of Bacillus cereus isolates from infant formula in China. Food Microbiol 62:46–50. https://doi.org/10.1016/j.fm.2016.09.007

    Article  CAS  PubMed  Google Scholar 

  27. Zahner V, Silva AC, Moraes GP, Mcintosh D, Id F (2013) Extended genetic analysis of Brazilian isolates of Bacillus cereus and Bacillus thuringiensis. Mem I Oswaldo Cruz 108(1):65–72. https://doi.org/10.1590/S0074-02762013000100011

    Article  CAS  Google Scholar 

  28. Zhang Y, Chen J, Feng C, Zhan L, Zhang J, Li Y, Yang Y, Chen H, Zhang Z, Zhang Y (2017) Quantitative prevalence, phenotypic and genotypic characteristics of Bacillus cereus isolated from retail infant foods in China. Foodborne Pathog Dis 42(10):564–572. https://doi.org/10.1089/fpd.2017.2287

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by the Doctor Scientific Research Start-up Fund of Henan University of Science and Technology (Grant No. 13480066), Science and Technology Project of Henan Province (Grant No. 172102110019), and National Natural Science Foundation of China (Grant No. 31702218).

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Authors and Affiliations

  1. College of Food and Bioengineering, Henan University of Science and Technology, Luoyang, 471023, China

    Peng Fei, Shengjuan Zhao, Tongxiang Yang, Jinle Xiang, Xi Chen, Lianxin Zhou & Mengdi Ji

  2. Anda Department of Animal Husbandry and Veterinary, Anda, 151400, China

    Xiujuan Yuan

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  1. Peng Fei
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Fei, P., Yuan, X., Zhao, S. et al. Prevalence and Genetic Diversity of Bacillus cereus Isolated from Raw Milk and Cattle Farm Environments. Curr Microbiol 76, 1355–1360 (2019). https://doi.org/10.1007/s00284-019-01741-5

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  • DOI: https://doi.org/10.1007/s00284-019-01741-5

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