Halobacteriovorax isolated from the Adriatic Sea to challenge Salmonella

Main Article Content

Silvia Pieralisi
Jasmine Hattab
Francesco Mosca
Gabriele Angelico
Laura Lanci
Donatella Ottaviani
Elena Rocchegiani
Pietro Giorgio Tiscar

Keywords

Bdellovibrio and like organisms, bivalves, Halobacteriovorax, Salmonella

Abstract

In the present study, we searched Halobacteriovorax strain preying upon Salmonella from the seawater of the Adriatic Sea. The Halobacteriovorax strain, named M7, was identified using 16S rRNA analysis. The M7 strain predation efficiency was tested against different Salmonella and non-Salmonella strains, all isolated from food matrices obtained from the Adriatic Sea. Finally, the M7 strain was exposed to Salmonella enterica subsp. enterica serovar Napoli in challenge tests to evaluate the killing of this specific prey over time. Double -layer agar plating technique was used to enumerate Halobacteriovorax and to evaluate its host specificity and predation efficiency. In the 103 predator/103 prey challenge test, M7 caused a decrease of Salmonella by about 2 log at 24 h compared to the control. In the 107 predator/104 prey challenge test, M7 caused a decrease of Salmonella by about 5 log at 24 h compared to the control, and good levels of decrease were obtained even at shorter times. Halobacteriovorax strains active against Salmonella are rarely present in the Adriatic Sea, Italy seawater. However, the isolate M7 showed high predatory efficiency towards a wide range of Salmonella strains. The presence of Salmonella in bivalves affects food safety since current decontamination processes are not always effective. M7 may represent a potential candidate for reducing and controlling Salmonella contamination in bivalves from harvesting to trade.

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References

2073/2005/EC, R. (2005). Commission Regulation (EC) No. 2073/2005 on microbiological criteria for foodstuffs. In E. Union (Ed.), 2073/2005. Brussels, Belgium The European parliament and the council of the European Union.

Amagliani, G., Brandi, G. and Schiavano, G.F. 2012. Incidence and role of Salmonella in seafood safety. Food Res. Inter. 45(2):780–788. 10.1016/j.foodres.2011.06.022

Andino, A. and Hanning, I. 2015. Salmonella enterica: survival, colonization, and virulence differences among serovars. The Scientific World Journal. 16. 10.1155/2015/520179

Baker, G.L. 2016. Food safety impacts from post-harvest processing procedures of molluscan shellfish. Foods. 5(2):29. 10.3390/foods5020029

Barile, N.B., Scopa, M., Nerone, E., Mascilongo, G., Recchi, S., Cappabianca, S., et al. 2009. Study of the efficacy of a closed cycle depuration system on bivalve molluscs. Vet. Ital. 45(4):555–560.

Bratanis, E., Andersson, T., Lood, R. and Bukowska-Faniband, E. 2020. Biotechnological potential of Bdellovibrio and like organisms and their secreted enzymes. Frontiers in Microbiol. 11:662. 10.3389/fmicb.2020.00662

Butt, A.A., Aldridge, K.E., Sanders C.V. Infections related to the ingestion of seafood Part I: viral and bacterial infections. The Lancet Infect. Dis. 4(4):201–212, 10.1016/S1473-3099(04)00969-7

Chen, H., Athar, R., Zheng, G. and Williams, H.N. 2011. Prey bacteria shape community structure of their predators. ISME Journal. 5:1314–1342. 10.1038/ismej.2011.4

Davidov, Y., Friedjung, A. and Jurkevitch, E. 2006. Structure analysis of a soil community of predatory bacteria using culture dependent and culture-independent methods reveals a hitherto undetected diversity of Bdellovibrio-and like organisms. Enviro. Microbiol. 8(9):1667–1673. 10.1111/j.1462-2920.2006.01052.x

EFSA & ECDC. 2016. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2015. EFSA Journal. 14(12):4634. 10.2903/j.efsa.2016.4634

FAO. 2005 Regional review on aquaculture development 6. Western-European Region–2005. FAO Fisheries Circular No. 1017/6 FIMA/C1017/6 ISSN 429-9329.

Iwamoto, M., Ayers, T., Mahon, B.E. and Swerdlow, D.L. 2010. Epidemiology of seafood-associated infections in the United States. Clin. Microbiol. Rev. 23:399–410. 10.1128/cmr.00059-09

Koval, S.F., Williams, H.N. and Stine, O.C. 2015. Reclassification of Bacteriovorax marinus as Halobacteriovorax marinus gen. nov., comb.nov. and Bacteriovorax litoralis as Halobacteriovorax litoralis comb. nov.; description of Halobacteriovoraceae fam. nov. in the class Deltaproteobacteria. Inter. J of Syst. and Evol. Microbiol. 65:593–597. 10.1099/ijs.0.070201-0

Li, H., Liu, C., Chen, L., Zhang, X. and Cai, J. 2011. Biological characterization of two marine Bdellovibrio-and-like organisms isolated from Daya bay of Shenzhen, China and their application in the elimination of Vibrio parahaemolyticus in oyster. Inter J of Food Microbiol. 151:36–43. 10.1016/j.ijfoodmicro.2011.07.036

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 Microbiol. 51:625–631. 10.1111/j.1472-765X.2010.02943.x

Morrison, C.M., Armstrong, A.E., Evans, S., Mild, R.M., Langdon, C.J., Joens, L.A. 2011. Survival of Salmonella Newport in oysters. Inter. J of Food Microbiol. 148:93–98. 10.1016/j.ijfoodmicro.2011.05.006

Novoslavskij, A., Terentjeva, M., Eizenberga, I., Valciņa, O., Bartkevičs, V., Bartkevičs, A. 2016. Major foodborne pathogens in fish and fish products: a review. Annals of Microbiol. 66:1–15. 10.1007/s13213-015-1102-5

Ottaviani, D., Chierichetti, S., Angelico, G., Forte, C., Rocchegiani, E., Manuali, E., et al. 2018. Halobacteriovorax isolated from marine water of the Adriatic Sea, Italy, as an effective predator of Vibrio parahaemolyticus, non-O1/O139 V. cholerae, V. vulnificus. J of Appl. Microbiol. 4:1199–1207. 10.1111/jam.14027

Ottaviani, D., Pieralisi, S., Chierichetti, S., Rocchegiani, E., Hattab, J., Mosca, F., et al. 2020a. Vibrio parahaemolyticus control in mussels by a Halobacteriovorax isolated from the Adriatic sea, Italy. Food Microbiol. 92:103600. 10.1016/j.fm.2020.103600

Ottaviani, D., Pieralisi, S., Rocchegiani, E., Latini, M., Leoni, F., Mosca, F., et al. 2020b. Vibrio parahaemolyticus-specific Halobacteriovorax from seawater of a mussel harvesting area in the Adriatic Sea: abundance, diversity, efficiency and relationship with the prey natural level. Frontiers in Microbiol. 11:1575. 10.3389/fmicb.2020.01575

Potasman, I., Paz, A. and Odeh, M. 2002. Infectious outbreaks associated with bivalve shellfish consumption: a worldwide perspective. Clin. Infec. Dis. 35:921–928. 10.1086/342330

Richards, G.P., Fay, J.P., Dickens, K.A., Parent, M.A., Soroka, D.S. and Boyd, E.F. 2012. Predatory bacteria as natural modulators of Vibrio parahaemolyticus and Vibrio vulnificus in seawater and oysters. Applied and Enviro. Microbiol. 78:7455–7466. 10.1128/AEM.01594-12

Richards, G.P., Watson, M.A., Boyd, E.F., Burkhardt, W.I.I.I., Lau, R., Uknalis, J., et al. 2013. Seasonal levels of the Vibrio predator Bacteriovorax in Atlantic, Pacific and Gulf Coast seawater. Inter. J of Microbiol. 2013:375371. 10.1155/2013/375371

Richards, G.P., Fay, J.P., Uknalis, J., Olanya, O.M. and Watson, M.A. 2016. Purification and host specificity of predatory Halobacteriovorax isolates from seawater. Applied and Enviro. Microbiol. 82:922–927. 10.1128/AEM.03136-15

Rippey, S.R. 1994. Infectious diseases associated with molluscan shellfish consumption. Clin. Microbiol. Rev. 7(4):419–425. 10.1128/CMR.7.4.419

Rubini, S., Galletti, G., D’Incau, M., Govoni, G., Boschetti, L., Berardelli, C., et al. 2018. Occurrence of Salmonella enterica subsp. enterica in bivalve molluscs and associations with Escherichia coli in molluscs and faecal coliforms in seawater. Food Control. 84:429–435. 10.1016/j.foodcont.2017.08.035

Sabbatucci, M., Dionisi, A.M., Pezzotti, P., Lucarelli, C., Barco, L., Mancin, M. and Luzzi, I. 2018. Molecular and epidemiologic analysis of reemergent Salmonella enterica Serovar Napoli, Italy, 2011-2015. Emerg. Infec. Dise. 24(3):562–565. 10.3201/eid2403.171178

Shatzkes, K., Connell, N.D. and Kadouri, D.E. 2017. Predatory bacteria: a new therapeutic approach for a post-antibiotic era. Future Microbiol. 12:469–472. 10.2217/fmb-2017-0021

Williams, H.N., Lymperopoulou, D.S., Athar, R., Chauhan, A., Dickerson, T.L., Chen, H., et al. 2016. Halobacteriovorax, an underestimated predator on bacteria: potential impact relative to viruses on bacterial mortality. The ISME Journal. 10:491–499; 10.1038/ismej.2015.129

Zahli, R., Soliveri, J., Abrini, J. Copa-Patiño, J.L., Nadia, A., Scheu, A-K., et al. 2021. Prevalence, typing and antimicrobial resistance of Salmonella isolates from commercial shellfish in the North coast of Morocco. World J Microbiol. and Biotechnol. 37:170. 10.1007/s11274-021-03136-w