Effectiveness of Bdellovibrio bacteriovorus to contain Escherichia coli on milk and temperature impact on predation dynamics
Main Article Content
Keywords
Bdellovibrio and like organisms, Bdellovibrio bacteriovorus, E. coli, milk
Abstract
We tested the predation of B. bacteriovorus against Escherichia coli in milk samples in three different experiments. In Experiment 1, the growth and predatory activity of B. bacteriovorus against E. coli in milk stored at 4°C were evaluated. In Experiment 2, the predatory activity of B. bacteriovorus against E. coli in the milk matrix was compared to the optimal one in the medium of choice. In Experiment 3, the influence of the native milk microbial community on the predation of B. bacteriovorus against E. coli experimentally added or indigenous grown at 4°C was tested. The predator increased at 4°C by about 1 Log in the first 48 hours and caused E. coli decrease by about 2 Log after 24 hours. The predator at 30°C reduced E. coli faster (3 Log after 6 hours) than at 4°C (2 Log after 24 hours). B. bacteriovorus at 30°C preyed on E. coli more in the nutrient broth than in the milk, with the most significant difference by about 4 Log after 48 hours. In raw milk contaminated only by the predator, it increased by about 1 Log after 48 hours at 4°C, suggesting that it preyed on indigenous microorganisms. B. bacteriovorus could find application in raw milk used as food or raw material during storage at 4°C to reduce the microbial load of spoilage and Shigatoxin-producing E. coli (STEC) strains of E. coli and therefore increase its shelf-life and healthiness.
References
Bonfiglio, G., Neroni, B., Radocchia, G., Marazzato, M., Pantanella, F. and Schippa, S., 2020a. Insight into the possible use of the predator Bdellovibrio bacteriovorus as a probiotic. Nutrients 12: 2252. 10.3390/nu12082252
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Boor, K.J., Wiedmann, M., Murphy, S. and Alcaine, S., 2017. A 100-year review: microbiology and safety of milk handling. Journal Dairy Science 100: 9933–9951. 10.3168/jds.2017-12969
Bratanis, E., Andersson, T., Lood, R. and Bukowska-Faniband, E., 2020. Biotechnological potential of Bdellovibrio and like organisms and their secreted enzymes. Frontiers Microbiology 11: 662. 10.3389/fmicb.2020.00662
Caprioli, A., Scavia, G. and Morabito, S., 2015. Public health microbiology of Shiga toxin-producing Escherichia coli. In: Vanessa, S. and Carolyn, J.H. (eds.) Enterohemorrhagic Escherichia coli and other Shiga toxin-producing E. coli. 1st ed. American Society of Microbiology, Washington, DC, pp. 263–295. 10.1128/microbiolspec.EHEC-0014-2013
Cassin, M.H., Lammerding, A.M., Todd, E.C.D., Ross, W. and McColl, R.S., 1998. Quantitative risk assessment for Escherichia coli O157:H7 in ground beef hamburgers. International Journal of Food Microbiology 41: 21–44. 10.1016/s0168-1605(98)00028-2
Dashiff, A., Junka, R.A., Libera, M. and Kadouri, D.E., 2011. Predation of human pathogens by the predatory bacteria Micavibrio aeruginosavorus and Bdellovibrio bacteriovorus. Journal of Applied Microbiology 110: 431–444. 10.1111/j.1365-2672.2010.04900.x
Dwidar, M., Monnappa, A.K. and Mitchell, R.J., 2012. The dual probiotic and antibiotic nature of Bdellovibrio bacteriovorus. BMB Reports 45: 71–78. 10.5483/BMBRep.2012.45.2.71
EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards), Koutsoumanis, K., Allende, A., Álvarez-Ordóñez, A., Bolton, D., Bover-Cid, S., et al. 2021. Scientific opinion on the role played by the environment in the emergence and spread of antimicrobial resistance (AMR) through the food chain. EFSA Journal 19(6): 6651, 188 pp. 10.2903/j.efsa.2021.6651
EFSA FEEDAP Panel (EFSA Panel on Additives and Products or Substances used in Animal Feed), Rychen, G., Aquilina, G., Azimonti, G., Bampidis, V., Bastos, M.L., et al. 2018. Guidance on the characterisation of microorganisms used as feed additives or as production organisms. EFSA Journal 16(3): 5206, 24 pp. 10.2903/j.efsa.2018.5206
European Community, 2004. Regulation (EC) No. 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules on the hygiene of foodstuffs. Available at: http://data.europa.eu/eli/reg/2004/853/oj.
Fratamico, P.M. and Cooke, P.H., 1996. Isolation of Bdellovibrios that prey on Escherichia coli O157:H7 and Salmonella species and application for removal of prey from stainless steel surfaces. Journal of Food Safety 16: 161–173. 10.1111/j.1745-4565.1996.tb00157.x
Fratamico, P.M. and Whiting, R.C., 1995. Ability of Bdellovibrio bacteriovorus 109 J to lyses gram-negative food-borne pathogenic and spoilage bacteria. Journal of Food Protection 58: 160–164. 10.4315/0362-028X-58.2.160
Iebba, V., Santangelo, F., Totino, V., Nicoletti, M., Gagliardi, A., De Biase, R.V., et al. 2013. Higher prevalence and abundance of Bdellovibrio bacteriovorus in the human gut of healthy subjects. PLoS One 8(4): e61608. 10.1371/journal.pone.0061608
ISO 16649-2:2001. Microbiology of food and animal feeding stuffs—horizontal method for the enumeration of beta-glucuronidase-positive Escherichia coli—part 2: colony-count technique at 44 degrees C using 5-bromo-4-chloro-3-indolyl beta-D-glucuronide. International Standards Organisation, Geneva.
ISO 6887-1:2017. Microbiology of food and feed—preparation of samples, initial suspension and dilutions for microbiological examination—part 1: general rules for the preparation of the initial suspension and decimal dilutions. International Standards Organisation, Geneva.
Italian Ministry of Health, Rome, 2009. Misure urgenti in materia di produzione, commercializzazione e vendita diretta di latte crudo per l’alimentazione umana. Italian Official Journal no. 10. Available at: https://www.gazzettaufficiale.it/eli/id/2009/01/14/09A00353/sg.
Italian Ministry of Health, Rome, 2013. Disposizioni urgenti per promuovere lo sviluppo del Paese mediante un più alto livello di tutela della salute. Italian Official Journal no. 24. Available at: https://www.gazzettaufficiale.it/eli/gu/2013/01/29/24/sg/pdf.
Jang, J., Hur, H.-G., Sadowsky, M.J., Byappanahalli, M.N., Yan, T. and Ishii, S., 2017. Environmental Escherichia coli: ecology and public health implications—a review. Journal of Applied Microbiology 123: 570–581. 10.1111/jam.13468
Kadouri, D. and O’Toole, G.A., 2005. Susceptibility of biofilms to Bdellovibrio bacteriovorus attack. Applied Environmental Microbiology 71: 4044–4051. 10.1128/AEM.71.7.4044-4051.2005
Kadouri, D.E., To, K., Shanks, R.M. and Doi, Y., 2013. Predatory bacteria: a potential ally against multidrug-resistant gram-negative pathogens. PLoS One 8(5): e63397. 10.1371/journal.pone.0063397
Lu, F. and Cai, J., 2010. The protective effect of Bdellovibrio-and-like organisms (BALO) on tilapia fish fillets against Salmonella enterica ssp. enterica serovar Typhimurium. Letters in Applied Microbiology 51: 625–631. 10.1111/j.1472-765X.2010.02943.x
Macdonald, L.E., Brett, J., Kelton, D., Majowicz, S.E., Snedeker, K. and Sargeant, K.J., 2011. A systematic review and meta-analysis of the effects of pasteurization on milk vitamins, and evidence for raw milk consumption and other health-related outcomes. Journal of Food Protection 74: 1814–1832. 10.4315/0362-028X.JFP-10-269
Markelova, N.Y., 2010. Predacious bacteria, Bdellovibrio with potential for biocontrol. International Journal of Hygiene and Environmental Health 213(6): 428–431. 10.1016/j.ijheh.2010.08.004
Ottaviani, D., Pieralisi, S., Angelico, G., Mosca, F., Tiscar, P.G., Rocchegiani, E., et al. 2019. Bdellovibrio bacteriovorus to control Escherichia coli on meat matrices. International Journal of Food Science and Technology 55(3): 988–994. 10.1111/ijfs.14355
Shemesh, Y. and Jurkevitch, E., 2004. Plastic phenotypic resistance to predation by Bdellovibrio and like organisms in bacterial prey. Environmental Microbiology 6: 12–18. 10.1046/j.1462-2920.2003.00530.x
Sockett, R.E., 2009. Predatory lifestyle of Bdellovibrio bacteriovorus. Annual Review of Microbiology 63: 523–539. 10.1146/annurev.micro.091208.073346
Stolp, H. and Starr, M.P., 1963. Bdellovibrio bacteriovorus gen. et sp. nov., a predatory, ectoparasitic and bacteriolytic microorganism. Antonie Van Leeuwenhoek 29: 217–248. 10.1007/BF02046064
Tremonte, P., Tipaldi, L., Succi, M., Pannella, G., Falasca, L., Capilongo, V., et al. 2014. Raw milk from vending machines: effects of boiling, microwave treatment, and refrigeration on microbiological quality. Journal Dairy Science 97: 3314–3320. 10.3168/jds.2013-7744
US Department of Agricultural (USDA), 2018. The project development of alternative intervention technologies for fresh or minimally processed foods Available at: https://www.ars.usda.gov/research/programs-projects/project/?accnNo=430150&fy=2018.
Vianna, P.C.B., Walter, E.H.M., Dias, M.E.F., Faria, J.A.F., Netto, F.M. and Gigante, M.L., 2012. Effect of addition of CO2 to raw milk on quality of UHT-treated milk. Journal of Dairy Science 95: 4256–4262. 10.3168/jds.2012-5387
Youdkes, D., Helman, Y., Burdman, S., Matan, O. and Jurkevitch, E., 2020. Potential control of potato soft rot disease by the obligate predators Bdellovibrio and like organisms. Applied Environmental Microbiology 86: e02543-19. 10.1128/AEM.02543-19.
Williams, H.N., Baer, M.L. and Tudor, J.J., 2005. Bdellovibrio Stolp and Starr. In: Garrity, G.M., Brenner, D.J., Krieg, N.R. and Staley, J.T. (eds.) Bergey’s manual of systematic bacteriology: the Proteobacteria, vol 2, part C. Springer, New York, NY, pp. 1040–1053. 10.1007/0-387-29298-5
Bonfiglio, G., Neroni, B., Radocchia, G., Pompilio, A., Mura, F., Trancassini, M., et al. 2020b. Growth control of adherent-invasive Escherichia coli (AIEC) by the predator bacteria Bdellovibrio bacteriovorus: a new therapeutic approach for Crohn’s disease patients. Microorganisms 8(1): 17. 10.3390/microorganisms8010017
Boor, K.J., Wiedmann, M., Murphy, S. and Alcaine, S., 2017. A 100-year review: microbiology and safety of milk handling. Journal Dairy Science 100: 9933–9951. 10.3168/jds.2017-12969
Bratanis, E., Andersson, T., Lood, R. and Bukowska-Faniband, E., 2020. Biotechnological potential of Bdellovibrio and like organisms and their secreted enzymes. Frontiers Microbiology 11: 662. 10.3389/fmicb.2020.00662
Caprioli, A., Scavia, G. and Morabito, S., 2015. Public health microbiology of Shiga toxin-producing Escherichia coli. In: Vanessa, S. and Carolyn, J.H. (eds.) Enterohemorrhagic Escherichia coli and other Shiga toxin-producing E. coli. 1st ed. American Society of Microbiology, Washington, DC, pp. 263–295. 10.1128/microbiolspec.EHEC-0014-2013
Cassin, M.H., Lammerding, A.M., Todd, E.C.D., Ross, W. and McColl, R.S., 1998. Quantitative risk assessment for Escherichia coli O157:H7 in ground beef hamburgers. International Journal of Food Microbiology 41: 21–44. 10.1016/s0168-1605(98)00028-2
Dashiff, A., Junka, R.A., Libera, M. and Kadouri, D.E., 2011. Predation of human pathogens by the predatory bacteria Micavibrio aeruginosavorus and Bdellovibrio bacteriovorus. Journal of Applied Microbiology 110: 431–444. 10.1111/j.1365-2672.2010.04900.x
Dwidar, M., Monnappa, A.K. and Mitchell, R.J., 2012. The dual probiotic and antibiotic nature of Bdellovibrio bacteriovorus. BMB Reports 45: 71–78. 10.5483/BMBRep.2012.45.2.71
EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards), Koutsoumanis, K., Allende, A., Álvarez-Ordóñez, A., Bolton, D., Bover-Cid, S., et al. 2021. Scientific opinion on the role played by the environment in the emergence and spread of antimicrobial resistance (AMR) through the food chain. EFSA Journal 19(6): 6651, 188 pp. 10.2903/j.efsa.2021.6651
EFSA FEEDAP Panel (EFSA Panel on Additives and Products or Substances used in Animal Feed), Rychen, G., Aquilina, G., Azimonti, G., Bampidis, V., Bastos, M.L., et al. 2018. Guidance on the characterisation of microorganisms used as feed additives or as production organisms. EFSA Journal 16(3): 5206, 24 pp. 10.2903/j.efsa.2018.5206
European Community, 2004. Regulation (EC) No. 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules on the hygiene of foodstuffs. Available at: http://data.europa.eu/eli/reg/2004/853/oj.
Fratamico, P.M. and Cooke, P.H., 1996. Isolation of Bdellovibrios that prey on Escherichia coli O157:H7 and Salmonella species and application for removal of prey from stainless steel surfaces. Journal of Food Safety 16: 161–173. 10.1111/j.1745-4565.1996.tb00157.x
Fratamico, P.M. and Whiting, R.C., 1995. Ability of Bdellovibrio bacteriovorus 109 J to lyses gram-negative food-borne pathogenic and spoilage bacteria. Journal of Food Protection 58: 160–164. 10.4315/0362-028X-58.2.160
Iebba, V., Santangelo, F., Totino, V., Nicoletti, M., Gagliardi, A., De Biase, R.V., et al. 2013. Higher prevalence and abundance of Bdellovibrio bacteriovorus in the human gut of healthy subjects. PLoS One 8(4): e61608. 10.1371/journal.pone.0061608
ISO 16649-2:2001. Microbiology of food and animal feeding stuffs—horizontal method for the enumeration of beta-glucuronidase-positive Escherichia coli—part 2: colony-count technique at 44 degrees C using 5-bromo-4-chloro-3-indolyl beta-D-glucuronide. International Standards Organisation, Geneva.
ISO 6887-1:2017. Microbiology of food and feed—preparation of samples, initial suspension and dilutions for microbiological examination—part 1: general rules for the preparation of the initial suspension and decimal dilutions. International Standards Organisation, Geneva.
Italian Ministry of Health, Rome, 2009. Misure urgenti in materia di produzione, commercializzazione e vendita diretta di latte crudo per l’alimentazione umana. Italian Official Journal no. 10. Available at: https://www.gazzettaufficiale.it/eli/id/2009/01/14/09A00353/sg.
Italian Ministry of Health, Rome, 2013. Disposizioni urgenti per promuovere lo sviluppo del Paese mediante un più alto livello di tutela della salute. Italian Official Journal no. 24. Available at: https://www.gazzettaufficiale.it/eli/gu/2013/01/29/24/sg/pdf.
Jang, J., Hur, H.-G., Sadowsky, M.J., Byappanahalli, M.N., Yan, T. and Ishii, S., 2017. Environmental Escherichia coli: ecology and public health implications—a review. Journal of Applied Microbiology 123: 570–581. 10.1111/jam.13468
Kadouri, D. and O’Toole, G.A., 2005. Susceptibility of biofilms to Bdellovibrio bacteriovorus attack. Applied Environmental Microbiology 71: 4044–4051. 10.1128/AEM.71.7.4044-4051.2005
Kadouri, D.E., To, K., Shanks, R.M. and Doi, Y., 2013. Predatory bacteria: a potential ally against multidrug-resistant gram-negative pathogens. PLoS One 8(5): e63397. 10.1371/journal.pone.0063397
Lu, F. and Cai, J., 2010. The protective effect of Bdellovibrio-and-like organisms (BALO) on tilapia fish fillets against Salmonella enterica ssp. enterica serovar Typhimurium. Letters in Applied Microbiology 51: 625–631. 10.1111/j.1472-765X.2010.02943.x
Macdonald, L.E., Brett, J., Kelton, D., Majowicz, S.E., Snedeker, K. and Sargeant, K.J., 2011. A systematic review and meta-analysis of the effects of pasteurization on milk vitamins, and evidence for raw milk consumption and other health-related outcomes. Journal of Food Protection 74: 1814–1832. 10.4315/0362-028X.JFP-10-269
Markelova, N.Y., 2010. Predacious bacteria, Bdellovibrio with potential for biocontrol. International Journal of Hygiene and Environmental Health 213(6): 428–431. 10.1016/j.ijheh.2010.08.004
Ottaviani, D., Pieralisi, S., Angelico, G., Mosca, F., Tiscar, P.G., Rocchegiani, E., et al. 2019. Bdellovibrio bacteriovorus to control Escherichia coli on meat matrices. International Journal of Food Science and Technology 55(3): 988–994. 10.1111/ijfs.14355
Shemesh, Y. and Jurkevitch, E., 2004. Plastic phenotypic resistance to predation by Bdellovibrio and like organisms in bacterial prey. Environmental Microbiology 6: 12–18. 10.1046/j.1462-2920.2003.00530.x
Sockett, R.E., 2009. Predatory lifestyle of Bdellovibrio bacteriovorus. Annual Review of Microbiology 63: 523–539. 10.1146/annurev.micro.091208.073346
Stolp, H. and Starr, M.P., 1963. Bdellovibrio bacteriovorus gen. et sp. nov., a predatory, ectoparasitic and bacteriolytic microorganism. Antonie Van Leeuwenhoek 29: 217–248. 10.1007/BF02046064
Tremonte, P., Tipaldi, L., Succi, M., Pannella, G., Falasca, L., Capilongo, V., et al. 2014. Raw milk from vending machines: effects of boiling, microwave treatment, and refrigeration on microbiological quality. Journal Dairy Science 97: 3314–3320. 10.3168/jds.2013-7744
US Department of Agricultural (USDA), 2018. The project development of alternative intervention technologies for fresh or minimally processed foods Available at: https://www.ars.usda.gov/research/programs-projects/project/?accnNo=430150&fy=2018.
Vianna, P.C.B., Walter, E.H.M., Dias, M.E.F., Faria, J.A.F., Netto, F.M. and Gigante, M.L., 2012. Effect of addition of CO2 to raw milk on quality of UHT-treated milk. Journal of Dairy Science 95: 4256–4262. 10.3168/jds.2012-5387
Youdkes, D., Helman, Y., Burdman, S., Matan, O. and Jurkevitch, E., 2020. Potential control of potato soft rot disease by the obligate predators Bdellovibrio and like organisms. Applied Environmental Microbiology 86: e02543-19. 10.1128/AEM.02543-19.
Williams, H.N., Baer, M.L. and Tudor, J.J., 2005. Bdellovibrio Stolp and Starr. In: Garrity, G.M., Brenner, D.J., Krieg, N.R. and Staley, J.T. (eds.) Bergey’s manual of systematic bacteriology: the Proteobacteria, vol 2, part C. Springer, New York, NY, pp. 1040–1053. 10.1007/0-387-29298-5
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