Bacteriophages: Combating Antimicrobial Resistance in Food-Borne Bacteria Prevalent in Agriculture
Abstract
:1. Introduction
2. Antimicrobial Resistance in Agriculture
3. Phage Infection and Replication
4. Bactericidal Effects of Bacteriophages Demonstrated in Agriculture
5. Phage Resistance
6. Advantages of Phage Therapy over Conventional Antibiotics
7. Concluding Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Wang, H.; McEntire, J.C.; Zhang, L.; Li, X.; Doyle, M. The transfer of antibiotic resistance from food to humans: Facts, implications and future directions. Rev. Sci. Tech. (Int. Off. Epizoot.) 2012, 31, 249–260. [Google Scholar] [CrossRef]
- De Been, M.; Lanza, V.F.; de Toro, M.; Scharringa, J.; Dohmen, W.; Du, Y.; van Schaik, W. Dissemination of cephalosporin resistance genes between Escherichia coli strains from farm animals and humans by specific plasmid lineages. PLoS Genet. 2014, 10, e1004776. [Google Scholar] [CrossRef] [PubMed]
- Checcucci, A.; Trevisi, P.; Luise, D.; Modesto, M.; Blasioli, S.; Braschi, I.; Mattarelli, P. Exploring the animal waste resistome: The spread of antimicrobial resistance genes through the use of livestock manure. Front. Microbiol. 2020, 11, 1416. [Google Scholar] [CrossRef] [PubMed]
- Antimicrobial Food Processing Aid Uses on Red Meat and Poultry Meat for Which Health Canada has Expressed No Objection. Available online: https://www.canada.ca/en/health-canada/corporate/contact-us/publications.html (accessed on 10 April 2021).
- Public Health Agency of Canada. Canadian Integrated Program for Antimicrobial Resistance; Annual Report 2017; PHAC: Ottawa ON, Canada, 2020.
- Public Health Agency of Canada. Canadian Integrated Program for Antimicrobial Resistance; Annual Report 2018; PHAC: Ottawa ON, Canada, 2020.
- World Health Organization. 2019 Antibacterial Agents in Clinical Development: An Analysis of the Antibacterial Clinical Development Pipeline; License: CC BY-NC-SA 3.0 IGO; World Health Organization: Geneva, Switzerland, 2019. [Google Scholar]
- Obaidat, M.M.; Stringer, A.P. Prevalence, molecular characterization, and antimicrobial resistance profiles of Listeria monocytogenes, Salmonella enterica, and Escherichia coli O157:H7 on dairy cattle farms in Jordan. J. Dairy Sci. 2019, 102, 8710–8720. [Google Scholar] [CrossRef] [PubMed]
- Rasheed, M.U.; Thajuddin, N.; Ahamed, P.; Teklemariam, Z.; Jamil, K. Antimicrobial drug resistance in strains of Escherichia coli isolated from food sources. Rev. Inst. Med. Trop. São Paulo 2014, 56, 341–346. [Google Scholar] [CrossRef]
- Gregova, G.; Kmet, V. Antibiotic resistance and virulence of Escherichia coli strains isolated from animal rendering plant. Sci. Rep. 2020, 10, 1–7. [Google Scholar]
- Varga, C.; Guerin, M.T.; Brash, M.L.; Slavic, D.; Boerlin, P.; Susta, L. Antimicrobial resistance in fecal Escherichia coli and Salmonella enterica isolates: A two-year prospective study of small poultry flocks in Ontario, Canada. BMC Vet. Res. 2019, 15, 464. [Google Scholar] [CrossRef]
- Gousia, P.; Economou, V.; Sakkas, H.; Leveidiotou, S.; Papadopoulou, C. Antimicrobial resistance of major foodborne pathogens from major meat products. Foodborne Pathog. Dis. 2011, 8, 27–38. [Google Scholar] [CrossRef]
- Oppliger, A.; Moreillon, P.; Charrière, N.; Giddey, M.; Morisset, D.; Sakwinska, O. Antimicrobial resistance of Staphylococcus aureus strains acquired by pig farmers from pigs. Appl. Environ. Microbiol. 2012, 78, 8010–8014. [Google Scholar] [CrossRef] [Green Version]
- Wang, D.; Wang, Z.; Yan, Z.; Wu, J.; Ali, T.; Li, J.; Lv, Y.; Han, B. Bovine mastitis Staphylococcus aureus: Antibiotic susceptibility profile, resistance genes and molecular typing of methicillin-resistant and methicillin-sensitive strains in China. Infect. Genet. Evol. 2015, 31, 9–16. [Google Scholar] [CrossRef] [PubMed]
- Jamali, H.; Paydar, M.; Radmehr, B.; Ismail, S.; Dadrasnia, A. Prevalence and antimicrobial resistance of Staphylococcus aureus isolated from raw milk and dairy products. Food Control 2015, 54, 383–388. [Google Scholar] [CrossRef]
- Li, T.; Lu, H.; Wang, X.; Gao, Q.; Dai, Y.; Shang, J.; Li, M. Molecular characteristics of Staphylococcus aureus causing bovine mastitis between 2014 and 2015. Front. Cell. Infect. Microbiol. 2017, 7, 127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- MacDougall, L.; Fyfe, M.; McIntyre, L.; Paccagnella, A.; Cordner, K.; Kerr, A.; Aramini, J. Frozen chicken nuggets and strips—A newly identified risk factor for Salmonella Heidelberg infection in British Columbia, Canada. J. Food Prot. 2004, 67, 1111–1115. [Google Scholar] [CrossRef]
- St Amand, J.A.; Otto, S.J.; Cassis, R.; Annett Christianson, C.B. Antimicrobial resistance of Salmonella enterica serovar Heidelberg isolated from poultry in Alberta. Avian Pathol. 2013, 42, 379–386. [Google Scholar] [CrossRef] [PubMed]
- Herrera-Sánchez, M.P.; Rodríguez-Hernández, R.; Rondón-Barragán, I.S. Molecular characterization of antimicrobial resistance and enterobacterial repetitive intergenic consensus-PCR as a molecular typing tool for Salmonella spp. isolated from poultry and humans. Vet. World 2020, 13, 1771. [Google Scholar] [CrossRef]
- Abd-Elghany, S.M.; Sallam, K.I.; Abd-Elkhalek, A.; Tamura, T. Occurrence, genetic characterization and antimicrobial resistance of Salmonella isolated from chicken meat and giblets. Epidemiol. Infect. 2015, 143, 997–1003. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liljebjelke, K.A.; Hofacre, C.L.; White, D.G.; Ayers, S.; Lee, M.D.; Maurer, J.J. Diversity of antimicrobial resistance phenotypes in Salmonella isolated from commercial poultry farms. Front. Vet. Sci. 2017, 4, 96. [Google Scholar] [CrossRef]
- Bronowski, C.; James, C.E.; Winstanley, C. Role of environmental survival in transmission of Campylobacter jejuni. FEMS Microbiol. Lett. 2014, 356, 8–19. [Google Scholar] [CrossRef] [Green Version]
- Elhadidy, M.; Miller, W.G.; Arguello, H.; Álvarez-Ordóñez, A.; Duarte, A.; Dierick, K.; Botteldoorn, N. Genetic basis and clonal population structure of antibiotic resistance in Campylobacter jejuni isolated from broiler carcasses in Belgium. Front. Microbiol. 2018, 9, 1014. [Google Scholar] [CrossRef] [Green Version]
- Abay, S.; Kayman, T.; Otlu, B.; Hizlisoy, H.; Aydin, F.; Ertas, N. Genetic diversity and antibiotic resistance profiles of Campylobacter jejuni isolates from poultry and humans in Turkey. Int. J. Food Microbiol. 2014, 178, 29–38. [Google Scholar] [CrossRef]
- Khan, J.A.; Rathore, R.S.; Abulreesh, H.H.; Qais, F.A.; Ahmad, I. Prevalence and antibiotic resistance profiles of Campylobacter jejuni isolated from poultry meat and related samples at retail shops in Northern India. Foodborne Pathog. Dis. 2018, 15, 218–225. [Google Scholar] [CrossRef]
- Agunos, A.; Léger, D.; Avery, B.P.; Parmley, E.J.; Deckert, A.; Carson, C.A.; Dutil, L. Ciprofloxacin-resistant Campylobacter spp. in retail chicken, western Canada. Emerg. Infect. Dis. 2013, 19, 1121. [Google Scholar] [CrossRef]
- United States Food and Drug Administration. 2008; Retail Meat Report: National Antimicrobial Resistance Monitoring System. Available online: http://www.fda.gov/downloads/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/NationalAntimicrobialResistanceMonitoringSystem/UCM237111.pdf (accessed on 29 March 2021).
- Ghosh, S.; LaPara, T.M. The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME J. 2007, 1, 191–203. [Google Scholar] [CrossRef] [Green Version]
- Kagambèga, A.; Lienemann, T.; Aulu, L.; Traoré, A.S.; Barro, N.; Siitonen, A.; Haukka, K. Prevalence and characterization of Salmonella enterica from the feces of cattle, poultry, swine and hedgehogs in Burkina Faso and their comparison to human Salmonella isolates. BMC Microbiol. 2013, 13, 253. [Google Scholar] [CrossRef] [Green Version]
- Montero, I.; Herrero, A.; Mendoza, M.C.; Rodicio, R.; Rodicio, M.R. Virulence-resistance plasmids (pUO-StVR2-like) in meat isolates of Salmonella enterica serovar Typhimurium. Food Res. Int. 2012, 45, 1025–1029. [Google Scholar] [CrossRef]
- Yoshizawa, N.; Usui, M.; Fukuda, A.; Asai, T.; Higuchi, H.; Okamoto, E.; Seki, K.; Takada, H.; Tamura, Y. Manure Compost Is a Potential Source of Tetracycline-Resistant Escherichia coli and Tetracycline Resistance Genes in Japanese Farms. Antibiotics 2020, 9, 76. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Usui, M.; Kawakura, M.; Yoshizawa, N.; San, L.L.; Nakajima, C.; Suzuki, Y.; Tamura, Y. Survival and prevalence of Clostridium difficile in manure compost derived from pigs. Anaerobe 2017, 43, 15–20. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.J.; Hu, H.W.; Chen, Q.L.; Singh, B.K.; Yan, H.; Chen, D.; He, J.Z. Transfer of antibiotic resistance from manure-amended soils to vegetable microbiomes. Environ. Int. 2019, 130, 104912. [Google Scholar] [CrossRef]
- Hesp, A.; Veldman, K.; van der Goot, J.; Mevius, D.; van Schaik, G. Monitoring antimicrobial resistance trends in commensal Escherichia coli from livestock, the Netherlands, 1998 to 2016. Eurosurveillance 2019, 24, 1800438. [Google Scholar] [CrossRef] [Green Version]
- Figura, G.; Budynek, P.; Dabrowska, K. Bacteriophage T4: Molecular aspects of bacterial cell infection and the role of capsid proteins. Postep. Hig. Med. Dosw. 2010, 64, 251–261. [Google Scholar]
- Baptista, C.; Santos, M.A.; São-José, C. Phage SPP1 reversible adsorption to Bacillus subtilis cell wall teichoic acids accelerates virus recognition of membrane receptor YueB. J. Bacteriol. 2008, 190, 4989–4996. [Google Scholar] [CrossRef] [Green Version]
- Taylor, N.M.; Prokhorov, N.S.; Guerrero-Ferreira, R.C.; Shneider, M.M.; Browning, C.; Goldie, K.N.; Stahlberg, H.; Leiman, P.G. Structure of the T4 baseplate and its function in triggering sheath contraction. Nature 2016, 533, 346–352. [Google Scholar] [CrossRef] [PubMed]
- Kanamaru, S.; Leiman, P.G.; Kostyuchenko, V.A.; Chipman, P.R.; Mesyanzhinov, V.V.; Arisaka, F.; Rossmann, M.G. Structure of the cell-puncturing device of bacteriophage T4. Nature 2002, 415, 553–557. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.; Tu, J.; Liu, J.; Molineux, I.J. Structural dynamics of bacteriophage P22 infection initiation revealed by cryo-electron tomography. Nat. Microbiol. 2019, 4, 1049–1056. [Google Scholar] [CrossRef]
- Capparelli, R.; Nocerino, N.; Iannaccone, M.; Ercolini, D.; Parlato, M.; Chiara, M.; Iannelli, D. Bacteriophage therapy of Salmonella enterica: A fresh appraisal of bacteriophage therapy. J. Infect. Dis. 2010, 201, 52–61. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nabergoj, D.; Modic, P.; Podgornik, A. Effect of bacterial growth rate on bacteriophage population growth rate. MicrobiologyOpen 2018, 7, e00558. [Google Scholar] [CrossRef] [Green Version]
- Abedon, S. Phage therapy pharmacology: Calculating phage dosing. Adv. Appl. Microbiol. 2011, 77, 1–40. [Google Scholar]
- Naghizadeh, M.; Torshizi MA, K.; Rahimi, S.; Engberg, R.M.; Dalgaard, T.S. Effect of serum anti-phage activity on colibacillosis control by repeated phage therapy in broilers. Vet. Microbiol. 2019, 234, 61–71. [Google Scholar] [CrossRef]
- Cerveny, K.E.; DePaola, A.; Duckworth, D.H.; Gulig, P.A. Phage therapy of local and systemic disease caused by Vibrio vulnificus in iron-dextran-treated mice. Infect. Immun. 2002, 70, 6251–6262. [Google Scholar] [CrossRef] [Green Version]
- Capparelli, R.; Parlato, M.; Borriello, G.; Salvatore, P.; Iannelli, D. Experimental phage therapy against Staphylococcus aureus in mice. Antimicrob. Agents Chemother. 2007, 51, 2765–2773. [Google Scholar] [CrossRef] [Green Version]
- Abedon, S.T. Phage therapy dosing: The problem(s) with multiplicity of infection (MOI). Bacteriophage 2016, 6, e1220348. [Google Scholar] [CrossRef] [Green Version]
- Morella, N.M.; Yang, S.C.; Hernandez, C.A.; Koskella, B. Rapid quantification of bacteriophages and their bacterial hosts in vitro and in vivo using droplet digital PCR. J. Virol. Methods 2018, 259, 18–24. [Google Scholar] [CrossRef] [PubMed]
- Kasman, L.M.; Kasman, A.; Westwater, C.; Dolan, J.; Schmidt, M.G.; Norris, J.S. Overcoming the phage replication threshold: A mathematical model with implications for phage therapy. J. Virol. 2002, 76, 5557–5564. [Google Scholar] [CrossRef] [Green Version]
- Payne, R.J.; Jansen, V.A. Understanding bacteriophage therapy as a density-dependent kinetic process. J. Theor. Biol. 2001, 208, 37–48. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, Y.; Shen, W.; Zhong, Q.; Chen, Q.; He, X.; Baker, J.L.; Xiong, K.; Jin, X.; Wang, J.; Hu, F.; et al. Development of a bacteriophage cocktail to constrain the emergence of phage-resistant Pseudomonas aeruginosa. Front. Microbiol. 2020, 11, 327. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Z.; Zheng, P.; Ji, W.; Fu, Q.; Wang, H.; Yan, Y.; Sun, J. SLPW: A virulent bacteriophage targeting methicillin-resistant Staphylococcus aureus in vitro and in vivo. Front. Microbiol. 2016, 7, 934. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Porter, J.; Anderson, J.; Carter, L.; Donjacour, E.; Paros, M. In vitro evaluation of a novel bacteriophage cocktail as a preventative for bovine coliform mastitis. J. Dairy Sci. 2016, 99, 2053–2062. [Google Scholar] [CrossRef] [PubMed]
- Yulinery, T.; Triana, E.; Suharna, N.; Nurhidayat, N. Isolation and anti-Escherichia coli biofilm activity of lytic bacteriophages isolated from water environment in vitro. In IOP Conference Series: Earth and Environmental Science; IOP: Bristol, UK, 2019; Volume 308, p. 012010. [Google Scholar]
- Guo, M.; Gao, Y.; Xue, Y.; Liu, Y.; Zeng, X.; Cheng, Y.; Ma, J.; Wang, H.; Sun, J.; Wang, Z.; et al. Bacteriophage Cocktails Protect Dairy Cows against Mastitis Caused By Drug Resistant Escherichia coli Infection. Front. Cell. Infect. Microbiol. 2021, 11, 555. [Google Scholar] [CrossRef] [PubMed]
- Ramirez, K.; Cazarez-Montoya, C.; Lopez-Moreno, H.S.; Castro-del Campo, N. Bacteriophage cocktail for biocontrol of Escherichia coli O157:H7: Stability and potential allergenicity study. PLoS ONE 2018, 13, e0195023. [Google Scholar] [CrossRef] [Green Version]
- Manohar, P.; Tamhankar, A.J.; Lundborg, C.S.; Ramesh, N. Isolation, characterization and in vivo efficacy of Escherichia phage myPSH1131. PLoS ONE 2018, 13, e0206278. [Google Scholar] [CrossRef]
- Clavijo, V.; Baquero, D.; Hernandez, S.; Farfan, J.C.; Arias, J.; Arévalo, A.; Donado-Godoy, P.; Vives-Flores, M. Phage cocktail SalmoFREE® reduces Salmonella on a commercial broiler farm. Poult. Sci. 2019, 98, 5054–5063. [Google Scholar] [CrossRef] [PubMed]
- Carter, C.D.; Parks, A.; Abuladze, T.; Li, M.; Woolston, J.; Magnone, J.; Senecal, A.; Kropinski, A.M.; Sulakvelidze, A. Bacteriophage cocktail significantly reduces Escherichia coli O157:H7 contamination of lettuce and beef, but does not protect against recontamination. Bacteriophage 2012, 2, 178–185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miguéis, S.; Saraiva, C.; Esteves, A. Efficacy of LISTEX P100 at different concentrations for reduction of Listeria monocytogenes inoculated in sashimi. J. Food Prot. 2017, 80, 2094–2098. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fernández, L.; Gutiérrez, D.; Rodríguez, A.; García, P. Application of bacteriophages in the agro-food sector: A long way toward approval. Front. Cell. Infect. Microbiol. 2018, 8, 296. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- EFSA Panel on Biological Hazards (BIOHAZ). Evaluation of the safety and efficacy of Listex™ P100 for reduction of pathogens on different ready-to-eat (RTE) food products. EFSA J. 2016, 14, e04565. [Google Scholar]
- Laforest, M.; Bisaillon, K.; Ciotola, M.; Cadieux, M.; Hébert, P.O.; Toussaint, V.; Svircev, A.M. Rapid identification of Erwinia amylovora and Pseudomonas syringae species and characterization of E. amylovora streptomycin resistance using quantitative PCR assays. Can. J. Microbiol. 2019, 65, 496–509. [Google Scholar] [CrossRef]
- Hwang, M.S.; Morgan, R.L.; Sarkar, S.F.; Wang, P.W.; Guttman, D.S. Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Appl. Environ. Microbiol. 2005, 71, 5182–5191. [Google Scholar] [CrossRef] [Green Version]
- Flores, O.; Retamales, J.; Núñez, M.; León, M.; Salinas, P.; Besoain, X.; Yañez, C.; Bastías, R. Characterization of bacteriophages against Pseudomonas syringae pv. actinidiae with potential use as natural antimicrobials in kiwifruit plants. Microorganisms 2020, 8, 974. [Google Scholar] [CrossRef]
- Rabiey, M.; Roy, S.R.; Holtappels, D.; Franceschetti, L.; Quilty, B.J.; Creeth, R.; Sundin, G.W.; Wagemans, J.; Lavigne, R.; Jackson, R.W. Phage biocontrol to combat Pseudomonas syringae pathogens causing disease in cherry. Microb. Biotechnol. 2020, 13, 1428–1445. [Google Scholar] [CrossRef]
- Adriaenssens, E.M.; van Vaerenbergh, J.; Vandenheuvel, D.; Dunon, V.; Ceyssens, P.J.; de Proft, M.; Kropinski, A.M.; Noben, J.P.; Maes, M.; Lavigne, R. T4-Related Bacteriophage LIMEstone Isolates for the Control of Soft Rot on Potato Caused by ‘Dickeya solani’. PLoS ONE 2012, 7, e33227. [Google Scholar] [CrossRef] [Green Version]
- Czajkowski, R.; Smolarska, A.; Ozymko, Z. The viability of lytic bacteriophage ΦD5 in potato-associated environments and its effect on Dickeya solani in potato (Solanum tuberosum L.) plants. PLoS ONE 2017, 12, e0183200. [Google Scholar] [CrossRef] [Green Version]
- Carstens, A.B.; Djurhuus, A.M.; Kot, W.; Jacobs-Sera, D.; Hatfull, G.F.; Hansen, L.H. Unlocking the Potential of 46 New Bacteriophages for Biocontrol of Dickeya solani. Viruses 2018, 10, 621. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ye, M.; Sun, M.; Zhao, Y.; Jiao, W.; Xia, B.; Liu, M.; Feng, Y.; Zhang, Z.; Huang, D.; Huang, R.; et al. Targeted inactivation of antibiotic-resistant Escherichia coli and Pseudomonas aeruginosa in a soil-lettuce system by combined polyvalent bacteriophage and biochar treatment. Environ. Pollut. 2018, 241, 978–987. [Google Scholar] [CrossRef] [PubMed]
- Kolenda, C.; Josse, J.; Medina, M.; Fevre, C.; Lustig, S.; Ferry, T.; Laurent, F. Evaluation of the activity of a combination of three bacteriophages alone or in association with antibiotics on Staphylococcus aureus embedded in biofilm or internalized in osteoblasts. Antimicrob. Agents Chemother. 2020, 64, e02231-19. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Sun, L.; Wei, R.; Gao, Q.; He, T.; Xu, C.; Liu, X.; Wang, R. Intracellular Staphylococcus aureus control by virulent bacteriophages within MAC-T bovine mammary epithelial cells. Antimicrob. Agents Chemother. 2017, 61, e01990-16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abedon, S.T. Spatial vulnerability: Bacterial arrangements, microcolonies, and biofilms as responses to low rather than high phage densities. Viruses 2012, 4, 663–687. [Google Scholar] [CrossRef] [Green Version]
- Islam, M.; Zhou, Y.; Liang, L.; Nime, I.; Liu, K.; Yan, T.; Wang, X.; Li, J. Application of a phage cocktail for control of Salmonella in foods and reducing biofilms. Viruses 2019, 11, 841. [Google Scholar] [CrossRef] [Green Version]
- Abdelrahman, F.; Easwaran, M.; Daramola, O.I.; Ragab, S.; Lynch, S.; Oduselu, T.J.; Khan, F.M.; Ayobami, A.; Adnan, F.; Torrents, E.; et al. Phage-Encoded Endolysins. Antibiotics 2021, 10, 124. [Google Scholar] [CrossRef]
- Grishin, A.V.; Karyagina, A.S.; Vasina, D.V.; Vasina, I.V.; Gushchin, V.A.; Lunin, V.G. Resistance to peptidoglycan-degrading enzymes. Crit. Rev. Microbiol. 2020, 46, 703–726. [Google Scholar] [CrossRef]
- Schmelcher, M.; Powell, A.M.; Camp, M.J.; Pohl, C.S.; Donovan, D.M. Synergistic streptococcal phage λSA2 and B30 endolysins kill streptococci in cow milk and in a mouse model of mastitis. Appl. Microbiol. Biotechnol. 2015, 99, 8475–8486. [Google Scholar] [CrossRef]
- Zhou, Y.; Zhang, H.; Bao, H.; Wang, X.; Wang, R. The lytic activity of recombinant phage lysin LysKΔamidase against staphylococcal strains associated with bovine and human infections in the Jiangsu province of China. Res. Vet. Sci. 2017, 111, 113–119. [Google Scholar] [CrossRef]
- Labrie, S.J.; Samson, J.E.; Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 2010, 8, 317–327. [Google Scholar] [CrossRef] [PubMed]
- Zhong, Z.; Emond-Rheault, J.-G.; Bhandare, S.; Lévesque, R.; Goodridge, L. Bacteriophage-Induced Lipopolysaccharide Mutations in Escherichia coli Lead to Hypersensitivity to Food Grade Surfactant Sodium Dodecyl Sulfate. Antibiotics 2020, 9, 552. [Google Scholar] [CrossRef] [PubMed]
- Knirel, Y.A.; Prokhorov, N.S.; Shashkov, A.S.; Ovchinnikova, O.G.; Zdorovenko, E.L.; Liu, B.; Letarov, A.V. Variations in O-antigen biosynthesis and O-acetylation associated with altered phage sensitivity in Escherichia coli 4 s. J. Bacteriol. 2015, 197, 905–912. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Szczepankowska, A. Role of CRISPR/cas system in the development of bacteriophage resistance. Adv. Virus Res. 2012, 82, 289–338. [Google Scholar]
- Deveau, H.; Barrangou, R.; Garneau, J.E.; Labonté, J.; Fremaux, C.; Boyaval, P.; Romero, D.A.; Horvath, P.; Moineau, S. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol. 2008, 190, 1390–1400. [Google Scholar] [CrossRef] [Green Version]
- Cobb, L.H.; Park, J.; Swanson, E.A.; Beard, M.C.; McCabe, E.M.; Rourke, A.S.; Seo, K.S.; Olivier, A.K.; Priddy, L.B. CRISPR–Cas9 modified bacteriophage for treatment of Staphylococcus aureus induced osteomyelitis and soft tissue infection. PLoS ONE 2019, 14, e0220421. [Google Scholar] [CrossRef] [Green Version]
- Burmeister, A.R.; Fortier, A.; Roush, C.; Lessing, A.J.; Bender, R.G.; Barahman, R.; Grant, R.; Chan, B.K.; Turner, P.E. Pleiotropy complicates a trade-off between phage resistance and antibiotic resistance. Proc. Natl. Acad. Sci. USA 2020, 117, 11207–11216. [Google Scholar] [CrossRef]
- Hao, G.; Chen, A.I.; Liu, M.; Zhou, H.; Egan, M.; Yang, X.; Kan, B.; Wang, H.; Goulian, M.; Zhu, J. Colistin resistance-mediated bacterial surface modification sensitizes phage infection. Antimicrob. Agents Chemother. 2019, 63, e01609-19. [Google Scholar] [CrossRef]
- Anand, T.; Virmani, N.; Bera, B.C.; Vaid, R.K.; Kumar, A.; Tripathi, B.N. Applications of Personalized Phage Therapy highlighting the importance of Bacteriophage Banks against Emerging Antimicrobial Resistance. Def. Life Sci. J. 2020, 5, 305–314. [Google Scholar] [CrossRef]
- Kim, S.G.; Giri, S.S.; Yun, S.; Kim, H.J.; Kim, S.W.; Kang, J.W.; Han, S.J.; Kwon, J.; Oh, W.T.; Jun, J.W.; et al. Synergistic phage–surfactant combination clears IgE-promoted Staphylococcus aureus aggregation in vitro and enhances the effect in vivo. Int. J. Antimicrob. Agents 2020, 56, 105997. [Google Scholar] [CrossRef] [PubMed]
- Połaska, M.; Sokołowska, B. Review bacteriophages—A new hope or a huge problem in the food industry. AIMS Microbiol. 2019, 5, 324–347. [Google Scholar] [CrossRef]
- Zulkarneev, E.R.; Aleshkin, A.V.; Kiseleva, I.A.; Rubalsky, E.O.; Rubalsky, O.V. Bacteriophage Cocktail Effectively Prolonging the Shelf-Life of Chilled Fish. Bull. Exp. Biol. Med. 2019, 167, 818–822. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.; Yang, J.; Zhu, X.; Lu, Y.; Xue, Y.; Lu, Z. Effects of Salmonella bacteriophage, nisin and potassium sorbate and their combination on safety and shelf life of fresh chilled pork. Food Control 2017, 73, 869–877. [Google Scholar] [CrossRef]
- Kahn, L.H.; Bergeron, G.; Bourassa, M.W.; De Vegt, B.; Gill, J.; Gomes, F.; Malouin, F.; Opengart, K.; Ritter, G.D.; Singer, R.S.; et al. From farm management to bacteriophage therapy: Strategies to reduce antibiotic use in animal agriculture. Ann. N. Y. Acad. Sci. 2019, 1441, 31–39. [Google Scholar] [CrossRef] [PubMed]
- Adesanya, O.; Oduselu, T.; Akin-Ajani, O.; Adewumi, O.M.; Ademowo, O.G. An exegesis of bacteriophage therapy: An emerging player in the fight against antimicrobial resistance. AIMS Microbiol. 2020, 6, 204–230. [Google Scholar] [CrossRef]
- Cromwell, G.L. Why and how antibiotics are used in swine production. Anim. Biotechnol. 2002, 13, 7–27. [Google Scholar] [CrossRef]
- Hays, V.W. Benefits and risks of antibiotics use in agriculture. In Agricultural Uses of Antibiotics; Moats, W.A., Ed.; American Chemical Society: Washington, DC, USA, 1986; pp. 74–87. [Google Scholar]
- Gordillo Altamirano, F.L.; Barr, J.J. Phage therapy in the postantibiotic era. Clin. Microbiol. Rev. 2019, 32, e00066-18. [Google Scholar] [CrossRef] [Green Version]
- Abedon, S.T.; García, P.; Mullany, P.; Aminov, R. Editorial: Phage therapy: Past, present and future. Front. Microbiol. 2017, 8. [Google Scholar] [CrossRef] [Green Version]
- Tomat, D.D.; Migliore, L.; Aquili, V.; Quiberoni, A.D.L.; Balagué, C. Phage biocontrol of enteropathogenic and shiga toxin-producing Escherichia coli in meat products. Front. Cell. Infect. Microbiol. 2013, 3, 20. [Google Scholar] [CrossRef] [Green Version]
- Dissanayake, U.; Ukhanova, M.; Moye, Z.D.; Sulakvelidze, A.; Mai, V. Bacteriophages reduce pathogenic Escherichia coli counts in mice without distorting gut microbiota. Front. Microbiol. 2019, 10, 1984. [Google Scholar] [CrossRef] [PubMed]
- Cani, P.D.; Possemiers, S.; Van de Wiele, T.; Guiot, Y.; Everard, A.; Rottier, O.; Geurts, L.; Naslain, D.; Neyrinck, A.; Lambert, D.M.; et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 2009, 58, 1091–1103. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cieplak, T.; Soffer, N.; Sulakvelidze, A.; Nielsen, D.S. A bacteriophage cocktail targeting Escherichia coli reduces E. coli in simulated gut conditions 2018, while preserving a nontargeted representative commensal normal microbiota. Gut Microbes 2018, 9, 391–399. [Google Scholar] [PubMed] [Green Version]
- Kim, K.H.; Ingale, S.L.; Kim, J.S.; Lee, S.H.; Lee, J.H.; Kwon, I.K.; Chae, B.J. Bacteriophage and probiotics both enhance the performance of growing pigs but bacteriophage are more effective. Anim. Feed. Sci. Technol. 2014, 196, 88–95. [Google Scholar] [CrossRef]
- Kim, J.S.; Hosseindoust, A.; Lee, S.H.; Choi, Y.H.; Kim, M.J.; Lee, J.H.; Kwon, I.K.; Chae, B.J. Bacteriophage cocktail and multistrain probiotics in the feed for weanling pigs: Effects on intestine morphology and targeted intestinal coliforms and Clostridium. Animal 2017, 11, 45–53. [Google Scholar] [CrossRef] [Green Version]
- Hosseindoust, A.R.; Lee, S.H.; Kim, J.S.; Choi, Y.H.; Noh, H.S.; Lee, J.H.; Jha, P.K.; Kwon, I.K.; Chae, B.J. Dietary bacteriophages as an alternative for zinc oxide or organic acids to control diarrhea and improve the performance of weanling piglets. Vet. Med. 2017, 62, 53–61. [Google Scholar] [CrossRef] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Au, A.; Lee, H.; Ye, T.; Dave, U.; Rahman, A. Bacteriophages: Combating Antimicrobial Resistance in Food-Borne Bacteria Prevalent in Agriculture. Microorganisms 2022, 10, 46. https://doi.org/10.3390/microorganisms10010046
Au A, Lee H, Ye T, Dave U, Rahman A. Bacteriophages: Combating Antimicrobial Resistance in Food-Borne Bacteria Prevalent in Agriculture. Microorganisms. 2022; 10(1):46. https://doi.org/10.3390/microorganisms10010046
Chicago/Turabian StyleAu, Arnold, Helen Lee, Terry Ye, Uday Dave, and Azizur Rahman. 2022. "Bacteriophages: Combating Antimicrobial Resistance in Food-Borne Bacteria Prevalent in Agriculture" Microorganisms 10, no. 1: 46. https://doi.org/10.3390/microorganisms10010046
APA StyleAu, A., Lee, H., Ye, T., Dave, U., & Rahman, A. (2022). Bacteriophages: Combating Antimicrobial Resistance in Food-Borne Bacteria Prevalent in Agriculture. Microorganisms, 10(1), 46. https://doi.org/10.3390/microorganisms10010046