Study of a lytic bacteriophage as a tool for the control of Salmonella Gallinarum in layer poultry Control bacteriófago de Salmonella Gallinarum en aves de postura
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Apr 16, 2024
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Abstract
One of the leading diseases affecting laying poultry in Argentina is fowl typhoid, caused by the pathogen Salmonella enterica serovar Gallinarum (S. Gallinarum). Although this disease was eradicated from industrial hatcheries in several developed countries, it is still present in commercial farms in Latin America, causing substantial economic losses due to high mortality rates, limited production of quality eggs, high veterinary costs, and the need to renovate infected facilities. To develop a new S. Gallinarum biocontrol method, in the present study, we characterized a bacteriophage in terms of host specificity, growth kinetics, and stability under different environmental conditions. The phage could infect an ample range of bacterial hosts and had no lytic activity against the vaccine strain 9R. Moreover, the phage was stable at pH 3, chloroform presence did not significantly reduce its titer, and its activity was
not affected by antibiotics or various chemical agents often used in aviculture. Application of a phage suspension on S. Gallinarum-contaminated surfaces resulted in a significant reduction of bacterial load (p < 0.05). These results show that lytic bacteriophages such as the one studied here are innovative alternatives with potential applications to control S. Gallinarum in laying poultry farms.
Keywords
Bacteriophage; Salmonella Gallinarum; fowl typhoid; laying poultry; biocontrol.
References
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doi: 10.1007/s00705-022-05694-2
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doi: 10.1128/AEM.03560-14
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[16] Andreatti Filho RL, Higgins JP, Higgins SE, Gaona G, et al. Ability of bacteriophages isolated from different sources to reduce Salmonella enterica serovar enteritidis in vitro and in vivo, Poultry Science, 86(9):1904-1909, 2007.
doi:10.1093/ps/86.9.1904
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doi:10.1093/ps/82.7.1108
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doi:10.1128/microbiolspec.PFS-0017-2017
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doi:10.1016/j.mimet.2016.07.027
[22] Prosdócimo F, Anselmo R, Olivetto N, Gomez I, et al., Evaluación de un bacteriófago para la prevención de Salmonella Gallinarum en aves de postura, Revista Argentina de Microbiología, 42 (1): 114, 2010.
[23] Kropinski AM, Mazzocco A, Waddell TE, Lingohr E, Johnson RP. Enumeration of bacteriophages by double agar overlay plaque assay, Methods in Molecular Biology, 501:69-76, 2009.
doi:10.1007/978-1-60327-164-6_7
[24] Mahmoud M, Askora A, Barakat AB, et al. Isolation and characterization of polyvalent bacteriophages infecting multi drug resistant Salmonella serovars isolated from broilers in Egypt. International Journal of Food Microbiology, 266:8-13, 2018.
doi:10.1016/j.ijfoodmicro.2017.11.009
[25] Mazzocco A, Waddell TE, Lingohr E, Johnson RP. Enumeration of bacteriophages using the small drop plaque assay system, Methods in Molecular Biology, 2009, 501:81-85.
doi:10.1007/978-1-60327-164-6_9
[26] Hyman P, Abedon ST. Practical methods for determining phage growth parameters, Methods in Molecular Biology, 501:175-202, 2009.
doi:10.1007/978-1-60327-164-6_18.
[27] Haq U, Chaudhry W, Andleeb S, et al. Isolation and Partial Characterization of a Virulent Bacteriophage IHQ1 Specific for Aeromonas punctata from Stream Water, Microbial Ecology, 63 (4):954–963, 2012.
doi:10.1007/s00248-011-9944-2
[28] Fernández Espinel C., V. Flores Dominick, M. Medina Morillo. Aislamiento y caracterización del bacteriófago Va1 específico a Vibrio Alginolyticus, Revista Peruana de Biología, 24(1):93-100, 2017.
doi:10.15381/rpb.v24i1.13103
[29] Manual of food quality control. 12. Quality assurance in the food control microbiological laboratory, FAO food and nutrition paper,14(12):1-154, 1991. http://www.fao.or
[30] Wang IN. Lysis timing and bacteriophage fitness, Genetics, 172 (1):17-26, 2006
[31] OIE. Organización Mundial de Sanidad Animal-Una sola salud
http://www.oie.int/es/para-los-periodistas/onehealth-es/
[32] Summers WC. Bacteriophage therapy, Annual Review of Microbiology, 55:437-451, 2001.
doi:10.1146/annurev.micro.55.1.437
[33] Wernicki A, Nowaczek A, Urban-Chmiel R. Bacteriophage therapy to combat bacterial infections in poultry, Virolgy Journal, 14(1):179, 2017.
doi:10.1186/s12985-017-0849-7
[34] [34] Joerger RD. Alternatives to antibiotics: bacteriocins, antimicrobial peptides and bacteriophages, Poultry Science, 82(4):640-647, 2003.
doi:10.1093/ps/82.4.640
[35] Lim TH, Lee DH, LeeYN, et al. Efficacy of bacteriophage therapy on horizontal transmission of Salmonella Gallinarum on commercial layer chickens, Avian Disease, 55(3):435-438, 2011.
doi:10.1637/9599-111210-Reg.1
[36] Matsuzaki S, Rashel M, Uchiyama J, et al. Bacteriophage therapy: a revitalized therapy against bacterial infectious diseases, Journal of Infection Chemotherapy, 11(5):211-219, 2005.
doi:10.1007/s10156-005-0408-9
[37] Bielke L, Higgins S, Donoghue A, Donoghue D, Hargis BM. Salmonella host range of bacteriophages that infect multiple genera, Poultry Science, 86(12):2536-2540, 2007.
doi:10.3382/ps.2007-00250
[38] Shin H, Lee JH, Kim H, Choi Y, Heu S, Ryu S. Receptor diversity and host interaction of bacteriophages infecting Salmonella enterica serovar Typhimurium, Public Library of Science (PLoS One), 7(8): e43392, 2012.
doi:10.1371/journal.pone.0043392
[39] Duckworth DH, Glenn J, McCorquodale DJ. Inhibition of bacteriophage replication by extrachromosomal genetic elements, Microbiological Reviews, 45(1):52-71, 1981.
doi:10.1128/mr.45.1.52-71.1981
[40] Calendar R, Inman R. Phage biology. Phages: Their Role in Bacterial Pathogenesis and Biotechnology, American Society for Microbiology Press, Washington DC, USA, 2005
[41] Kutter E, R. Raya R, Carlson K. Bacteriophages: Biology and Applications, CRC Press, Boca Raton, Florida, USA, 2005
[42] Singh A, Arya SK, Glass N, Hanifi-Moghaddam P, et al. Bacteriophage tailspike proteins as molecular probes for sensitive and selective bacterial detection, Biosensors and Bioelectronics, 26(1):131-8, 2010.
doi:10.1016/j.bios.2010.05.024.
[43] Hofer B, Ruge, M, Dreiseikelmann B. The Superinfection Exclusion Gene (sieA) of Bacteriophage P22: Identification and Overexpression of the Gene and Localization of the Gene Product, Journal of Bacteriology, 177(11):3080-3086, 1995.
doi:10.1128/jb.177.11.3080-3086.1995.
[44] Labrie SJ, Samson JE, Moineau S. Bacteriophage resistance mechanisms, Nature Reviews Microbiology, 8(5):317-327, 2010.
doi: 10.1038/nrmicro2315 PMID: 20348932.
[45] Hong SS, Jeong J, Lee J, Kim S, et al. Therapeutic effects of bacteriophages against Salmonella Gallinarum infection in chickens, Journal of Microbiology Biotechnology, 23(10): 1478-1483, 2013.
doi:10.4014/jmb.1304.04067
[46] Carey-Smith GV, Billington C, Cornelius AJ, Hudson JA, Heinemann JA. Isolation and characterization of bacteriophages infecting Salmonella spp., FEMS Microbiology Letters, 258(2):182-186, 2006.
doi:10.1111/j.1574-6968.2006.00217.x
[47] Pereira C, Moreirinha C, Lewicka M, et al. Bacteriophages with potential to inactivate Salmonella Typhimurium: Use of single phage suspensions and phage cocktails, Virus Research, 220:179-192, 2016.
doi:10.1016/j.virusres.2016.04.020
[48] Kasman LM, Kasman A, Westwater C, Dolan J, et al. Overcoming the phage replication threshold: a mathematical model with implications for phage therapy, Journal of Virology, 76(11):5557-5564, 2002.
doi:10.1128/jvi.76.11.5557-5564.2002
[49] Hyman P, Abedon ST. Practical methods for determining phage growth parameters, Methods in Molecular Biology, 501:175-202, 2009.
doi:10.1007/978-1-60327-164-6_18
[50] Jończyk E, Kłak M, Międzybrodzki R, Górski A. The influence of external factors on bacteriophages–review. Folia Microbiologica, 56(3):191-200, 2011.
doi:10.1007/s12223-011-0039-8
[51] Huang C, Virk SM, Shi J, et al. Isolation, Characterization, and Application of Bacteriophage LPSE1 Against Salmonella enterica in Ready to Eat (RTE) Foods, Frontiers in Microbiology, 9:1046, 2018.
doi:10.3389/fmicb.2018.01046
[52] Tang F, Zhang P, Zhang Q, et al. Isolation and characterization of a broad-spectrum phage of multiple drug resistant Salmonella and its therapeutic utility in mice, Microbial Pathogenesis, 126:193-198, 2019.
doi:10.1016/j.micpath.2018.10.042
[2] Regulation (EC) N◦ 1831/2003 of the European parliament and of the council of 22 September 2003 on additives for use in animal nutrition. Official Journal of the European Communities, 268: 29-43, 2003.
[3] Steiner, T. Managing gut health: natural growth promoters as a key to animal performance, Nottingham University Press, UK 2006.
[4] d’Hérelle F. Sur un microbe invisible antagoniste des bacilles dysentériques. Acta Kravsi, 2: 40-42, 1961.
[5] Twort FW. An investigation on the nature of ultramicroscopic viruses. Lancet, 2: 1241–1243, 1915.
doi:10.1016/S0140-6736(01)20383-3.
[6] Walker PJ, Siddell SG, Lefkowitz EJ, et al. Recent changes to virus taxonomy ratified by the International Committee on Taxonomy of Viruses (2022). Archives of Virology,167(11):2429-2440, 2022.
doi:10.1007/s00705-022-05516-5
[7] Turner D, Shkoporov AN, Lood C, et al. Abolishment of morphology-based taxa and change to binomial species names: 2022
axonomy update of the ICTV bacterial viruses subcommittee. Archives of Virology. 168(2):74, 2023
doi: 10.1007/s00705-022-05694-2
[8] Gutiérrez D, Vandenheuvel D, Martínez B, Rodríguez A, et al. Two phages, phiIPLA-RODI and phBiIPLA-C1C, lyse mono- and dual-species staphylococcal biofilms, Appllied and Environmental Microbiology, 81: 3336-48, 2015.
doi: 10.1128/AEM.03560-14
[9] Khalifa L, BroshY, Gelman D, Coppenhagen-Glazer S, et al. Targeting Enterococcus faecalis biofilms with phage therapy, Appllied and Environmental Microbiology, 81: 2696-2705, 2015.
doi: 10.1128/AEM.00096-15
[10] Nakai T, Sugimoto R, Park K-H, Matsuoka S, et al. Protective effects of bacteriophage on experimental Lactococcus garvieae infection in yellowtail, Diseases of Aquatic Organism, 37(1): 33-41, 1999.
doi: 10.3354/dao037033
[11] Smith HW, Huggins MB, Shaw KM. The control of experimental Escherichia coli diarrhea in calves by means of bacteriophages, Journal of General Microbiology ,133:1111-1126, 1987.
doi:10.1099/00221287-133-5-1111
[12] Smith H. W., Huggins M. B. Effectiveness of phages in treating experimental Escherichia coli diarrhea in calves, piglets and lambs, Journal of General Microbiology,129:2659-2675, 1983.
doi:10.1099/00221287-129-8-2659
[13] Stanford K, Niu YD, Johnson R. Oral delivery systems for encapsulated bacteriophages targeted at Escherichia coli O157:H7 in feedlot cattle, Journal of Food Protection, 73: 1304-1312, 2010
doi:10.4315/0362-028x-73.7.1304
[14] Atterbury RJ, Van Bergen MAP, Ortiz F, Lovell MA, et al. Bacteriophage therapy to reduce Salmonella colonization of broiler chickens, Appllied and Environmental Microbiology, 73(14):4543-4549, 2007.
doi:10.1128/AEM.00049-07
[15] Wagenaar JA, Bergen MAPV, Mueller MA, Wassenaar TM, Carlton RM. Phage therapy reduces Campylobacter jejuni colonization in broilers, Veterinary Microbiology, 109(3-4):275-283, 2005.
doi:10.1016/j.vetmic.2005.06.002
[16] Andreatti Filho RL, Higgins JP, Higgins SE, Gaona G, et al. Ability of bacteriophages isolated from different sources to reduce Salmonella enterica serovar enteritidis in vitro and in vivo, Poultry Science, 86(9):1904-1909, 2007.
doi:10.1093/ps/86.9.1904
[17] Huff WE, Huff GR, Rath NC, Balog JM, Donoghue AM. Bacteriophage treatment of a severe Escherichia coli respiratory infection in broiler chickens, Avian Disease, 47(4):1399-1405, 2003.
doi:10.1637/7041
[18] Huff WE, Huff GR, Rath NC, Balog JM, Donoghue AM. Evaluation of aerosol spray and intramuscular injection of bacteriophage to treat an Escherichia coli respiratory infection, Poultry Science, 82(7):1108-1112, 2003.
doi:10.1093/ps/82.7.1108
[19] Huff WE, Huff GR, Rath NC, Balog JM, Donoghue AM. Prevention of Escherichia coli infection in broiler chickens with a bacteriophage aerosol spray, Poultry Science, 81(10):1486- 1491, 2002.
doi:10.1093/ps/81.10.1486
[20] Colavecchio A, Goodridge LD. Phage Therapy Approaches to Reducing Pathogen Persistence and Transmission in Animal Production Environments: Opportunities and Challenges, Microbiology Spectrum Journal 5(3):5.3.25, 2017.
doi:10.1128/microbiolspec.PFS-0017-2017
[21] Cooper IR. A review of current methods using bacteriophages in live animals, food and animal products intended for human consumption, Journal of Microbiological Methods, 130: 38-47, 2016.
doi:10.1016/j.mimet.2016.07.027
[22] Prosdócimo F, Anselmo R, Olivetto N, Gomez I, et al., Evaluación de un bacteriófago para la prevención de Salmonella Gallinarum en aves de postura, Revista Argentina de Microbiología, 42 (1): 114, 2010.
[23] Kropinski AM, Mazzocco A, Waddell TE, Lingohr E, Johnson RP. Enumeration of bacteriophages by double agar overlay plaque assay, Methods in Molecular Biology, 501:69-76, 2009.
doi:10.1007/978-1-60327-164-6_7
[24] Mahmoud M, Askora A, Barakat AB, et al. Isolation and characterization of polyvalent bacteriophages infecting multi drug resistant Salmonella serovars isolated from broilers in Egypt. International Journal of Food Microbiology, 266:8-13, 2018.
doi:10.1016/j.ijfoodmicro.2017.11.009
[25] Mazzocco A, Waddell TE, Lingohr E, Johnson RP. Enumeration of bacteriophages using the small drop plaque assay system, Methods in Molecular Biology, 2009, 501:81-85.
doi:10.1007/978-1-60327-164-6_9
[26] Hyman P, Abedon ST. Practical methods for determining phage growth parameters, Methods in Molecular Biology, 501:175-202, 2009.
doi:10.1007/978-1-60327-164-6_18.
[27] Haq U, Chaudhry W, Andleeb S, et al. Isolation and Partial Characterization of a Virulent Bacteriophage IHQ1 Specific for Aeromonas punctata from Stream Water, Microbial Ecology, 63 (4):954–963, 2012.
doi:10.1007/s00248-011-9944-2
[28] Fernández Espinel C., V. Flores Dominick, M. Medina Morillo. Aislamiento y caracterización del bacteriófago Va1 específico a Vibrio Alginolyticus, Revista Peruana de Biología, 24(1):93-100, 2017.
doi:10.15381/rpb.v24i1.13103
[29] Manual of food quality control. 12. Quality assurance in the food control microbiological laboratory, FAO food and nutrition paper,14(12):1-154, 1991. http://www.fao.or
[30] Wang IN. Lysis timing and bacteriophage fitness, Genetics, 172 (1):17-26, 2006
[31] OIE. Organización Mundial de Sanidad Animal-Una sola salud
http://www.oie.int/es/para-los-periodistas/onehealth-es/
[32] Summers WC. Bacteriophage therapy, Annual Review of Microbiology, 55:437-451, 2001.
doi:10.1146/annurev.micro.55.1.437
[33] Wernicki A, Nowaczek A, Urban-Chmiel R. Bacteriophage therapy to combat bacterial infections in poultry, Virolgy Journal, 14(1):179, 2017.
doi:10.1186/s12985-017-0849-7
[34] [34] Joerger RD. Alternatives to antibiotics: bacteriocins, antimicrobial peptides and bacteriophages, Poultry Science, 82(4):640-647, 2003.
doi:10.1093/ps/82.4.640
[35] Lim TH, Lee DH, LeeYN, et al. Efficacy of bacteriophage therapy on horizontal transmission of Salmonella Gallinarum on commercial layer chickens, Avian Disease, 55(3):435-438, 2011.
doi:10.1637/9599-111210-Reg.1
[36] Matsuzaki S, Rashel M, Uchiyama J, et al. Bacteriophage therapy: a revitalized therapy against bacterial infectious diseases, Journal of Infection Chemotherapy, 11(5):211-219, 2005.
doi:10.1007/s10156-005-0408-9
[37] Bielke L, Higgins S, Donoghue A, Donoghue D, Hargis BM. Salmonella host range of bacteriophages that infect multiple genera, Poultry Science, 86(12):2536-2540, 2007.
doi:10.3382/ps.2007-00250
[38] Shin H, Lee JH, Kim H, Choi Y, Heu S, Ryu S. Receptor diversity and host interaction of bacteriophages infecting Salmonella enterica serovar Typhimurium, Public Library of Science (PLoS One), 7(8): e43392, 2012.
doi:10.1371/journal.pone.0043392
[39] Duckworth DH, Glenn J, McCorquodale DJ. Inhibition of bacteriophage replication by extrachromosomal genetic elements, Microbiological Reviews, 45(1):52-71, 1981.
doi:10.1128/mr.45.1.52-71.1981
[40] Calendar R, Inman R. Phage biology. Phages: Their Role in Bacterial Pathogenesis and Biotechnology, American Society for Microbiology Press, Washington DC, USA, 2005
[41] Kutter E, R. Raya R, Carlson K. Bacteriophages: Biology and Applications, CRC Press, Boca Raton, Florida, USA, 2005
[42] Singh A, Arya SK, Glass N, Hanifi-Moghaddam P, et al. Bacteriophage tailspike proteins as molecular probes for sensitive and selective bacterial detection, Biosensors and Bioelectronics, 26(1):131-8, 2010.
doi:10.1016/j.bios.2010.05.024.
[43] Hofer B, Ruge, M, Dreiseikelmann B. The Superinfection Exclusion Gene (sieA) of Bacteriophage P22: Identification and Overexpression of the Gene and Localization of the Gene Product, Journal of Bacteriology, 177(11):3080-3086, 1995.
doi:10.1128/jb.177.11.3080-3086.1995.
[44] Labrie SJ, Samson JE, Moineau S. Bacteriophage resistance mechanisms, Nature Reviews Microbiology, 8(5):317-327, 2010.
doi: 10.1038/nrmicro2315 PMID: 20348932.
[45] Hong SS, Jeong J, Lee J, Kim S, et al. Therapeutic effects of bacteriophages against Salmonella Gallinarum infection in chickens, Journal of Microbiology Biotechnology, 23(10): 1478-1483, 2013.
doi:10.4014/jmb.1304.04067
[46] Carey-Smith GV, Billington C, Cornelius AJ, Hudson JA, Heinemann JA. Isolation and characterization of bacteriophages infecting Salmonella spp., FEMS Microbiology Letters, 258(2):182-186, 2006.
doi:10.1111/j.1574-6968.2006.00217.x
[47] Pereira C, Moreirinha C, Lewicka M, et al. Bacteriophages with potential to inactivate Salmonella Typhimurium: Use of single phage suspensions and phage cocktails, Virus Research, 220:179-192, 2016.
doi:10.1016/j.virusres.2016.04.020
[48] Kasman LM, Kasman A, Westwater C, Dolan J, et al. Overcoming the phage replication threshold: a mathematical model with implications for phage therapy, Journal of Virology, 76(11):5557-5564, 2002.
doi:10.1128/jvi.76.11.5557-5564.2002
[49] Hyman P, Abedon ST. Practical methods for determining phage growth parameters, Methods in Molecular Biology, 501:175-202, 2009.
doi:10.1007/978-1-60327-164-6_18
[50] Jończyk E, Kłak M, Międzybrodzki R, Górski A. The influence of external factors on bacteriophages–review. Folia Microbiologica, 56(3):191-200, 2011.
doi:10.1007/s12223-011-0039-8
[51] Huang C, Virk SM, Shi J, et al. Isolation, Characterization, and Application of Bacteriophage LPSE1 Against Salmonella enterica in Ready to Eat (RTE) Foods, Frontiers in Microbiology, 9:1046, 2018.
doi:10.3389/fmicb.2018.01046
[52] Tang F, Zhang P, Zhang Q, et al. Isolation and characterization of a broad-spectrum phage of multiple drug resistant Salmonella and its therapeutic utility in mice, Microbial Pathogenesis, 126:193-198, 2019.
doi:10.1016/j.micpath.2018.10.042
How to Cite
Ortiz, X., Gismondi, M. I., & Barrios, H. (2024). Study of a lytic bacteriophage as a tool for the control of Salmonella Gallinarum in layer poultry: Control bacteriófago de Salmonella Gallinarum en aves de postura. Universitas Scientiarum, 29(1), 57–80. https://doi.org/10.11144/Javeriana.SC291.soal
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Section
Veterinary Microbiology
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