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Phage-mediated dissemination of virulence factors in pathogenic bacteria facilitated by antibiotic growth promoters in animals: a perspective

Published online by Cambridge University Press:  29 November 2017

Migma Dorji Tamang
Affiliation:
School of Public Health, University of Alberta, Edmonton, Alberta, Canada
Hoon Sunwoo
Affiliation:
Faculty of Pharmacy and Pharmaceutical Sciences, University of Alberta, Edmonton, Alberta, Canada
Byeonghwa Jeon*
Affiliation:
School of Public Health, University of Alberta, Edmonton, Alberta, Canada
*
*Corresponding author. E-mail: [email protected]

Abstract

Addition of sub-therapeutic antibiotics to the feed of food-producing animals for growth promotion and disease prevention has become a common agricultural practice in many countries. The emergence of antibiotic-resistant pathogens is a looming concern associated with the use of antibiotic growth promoters (AGPs) around the world. In addition, some studies have shown that AGPs may not only affect antibiotic resistance but may also stimulate the dissemination of virulence factors via bacteriophages. Although only a few studies are currently available in the literature regarding this topic, in this article we endeavor to provide a perspective about how AGPs would impact the transmission of virulence factors by horizontal gene transfer via phages in a few pathogenic bacterial species significant to livestock production.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2017 

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References

Aarestrup, FM (2015). The livestock reservoir for antimicrobial resistance: a personal view on changing patterns of risks, effects of interventions and the way forward. Philosophical Transactions of the Royal Society B 370: 20140085.Google Scholar
Agersø, Y, Wulff, G, Vaclavik, E, Halling-Sørensen, B and Jensen, LB (2006). Effect of tetracycline residues in pig manure slurry on tetracycline-resistant bacteria and resistance gene tet (M) in soil microcosms. Environment International 32: 876882.Google Scholar
Allen, HK, Looft, T, Bayles, DO, Humphrey, S, Levine, UY, Alt, D and Stanton, TB (2011). Antibiotics in feed induce prophages in swine fecal microbiomes. mBio 2: 00260-11.CrossRefGoogle ScholarPubMed
Allison, HE (2007). Stx-phages: drivers and mediators of the evolution of STEC and STEC-like pathogens. Future Microbiology 2: 165174.Google Scholar
Andersson, DI and Hughes, D (2014). Microbiological effects of sublethal levels of antibiotics. Nature Reviews Microbiology 12: 465.Google Scholar
Bager, F, Madsen, M, Christensen, J and Aarestrup, FM (1997). Avoparcin used as a growth promoter is associated with the occurrence of vancomycin-resistant Enterococcus faecium on Danish poultry and pig farms. Preventive Veterinary Medicine 31: 95112.CrossRefGoogle ScholarPubMed
Bearson, BL and Brunelle, BW (2015). Fluoroquinolone induction of phage-mediated gene transfer in multidrug-resistant Salmonella. International Journal of Antimicrobial Agents 46: 201204.Google Scholar
Bearson, BL, Allen, HK, Brunelle, BW, Lee, IS, Casjens, SR and Stanton, TB (2014). The agricultural antibiotic carbadox induces phage-mediated gene transfer in Salmonella. Frontiers in Microbiology 5.Google Scholar
Betley, MJ and Mekalanos, JJ (1985). Staphylococcal enterotoxin A is encoded by phage. Science 229: 185188.Google Scholar
Böhnel, H and Gessler, F (2005). Botulinum toxins – cause of botulism and systemic diseases? Veterinary Research Communications 29: 313345.Google Scholar
Casey, JA, Curriero, FC, Cosgrove, SE, Nachman, KE and Schwartz, BS (2013). High-density livestock operations, crop field application of manure, and risk of community-associated methicillin-resistant Staphylococcus aureus infection in Pennsylvania. JAMA Internal Medicine 173: 19801990.Google Scholar
Castanon, J (2007). History of the use of antibiotic as growth promoters in European poultry feeds. Poultry Science 86: 24662471.Google Scholar
Chantziaras, I, Boyen, F, Callens, B and Dewulf, J (2013). Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: a report on seven countries. Journal of Antimicrobial Chemotherapy 69: 827834.CrossRefGoogle ScholarPubMed
Cho, I, Yamanishi, S, Cox, L, Methé, BA, Zavadil, J, Li, K, Gao, Z, Mahana, D, Raju, K, Teitler, I and Li, H (2012). Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488: 621626.Google Scholar
Cornick, NA, Helgerson, AF, Mai, V, Ritchie, JM and Acheson, DW (2006). In vivo transduction of an Stx-encoding phage in ruminants. Applied and Environmental Microbiology 72: 50865088.CrossRefGoogle ScholarPubMed
Critchley, EM (1991). A comparison of human and animal botulism: a review. Journal of the Royal Society of Medicine 84: 295298.Google Scholar
Dahlenborg, M, Borch, E and Rådström, P (2001). Development of a combined selection and enrichment PCR procedure for Clostridium botulinum types B, E, and F and its use to determine prevalence in fecal samples from slaughtered pigs. Applied and Environmental Microbiology 67: 47814788.Google Scholar
Davis, TK, McKee, R, Schnadower, D and Tarr, PI (2013). Treatment of Shiga toxin-producing Escherichia coli infections. Infectious Disease Clinics of North America 27: 577597.Google Scholar
Diard, M, Bakkeren, E, Cornuault, JK, Moor, K, Hausmann, A, Sellin, ME, Loverdo, C, Aertsen, A, Ackermann, M, De Paepe, M and Slack, E (2017). Inflammation boosts bacteriophage transfer between Salmonella spp. Science 355: 12111215.Google Scholar
Diep, BA, Gill, SR, Chang, RF, Phan, TH, Chen, JH, Davidson, MG, Lin, F, Lin, J, Carleton, HA, Mongodin, EF and Sensabaugh, GF (2006). Complete genome sequence of USA300, an epidemic clone of community-acquired methicillin-resistant Staphylococcus aureus. The Lancet 367: 731739.Google Scholar
Dutil, L, Irwin, R, Finley, R, Ng, LK, Avery, B, Boerlin, P, Bourgault, AM, Cole, L, Daignault, D, Desruisseau, A and Demczuk, W (2010). Ceftiofur resistance in Salmonella enterica serovar Heidelberg from chicken meat and humans, Canada. Emerging Infectious Diseases 16: 48.Google Scholar
Eklund, MW and Poysky, FT (1974). Interconversion of type C and D strains of Clostridium botulinum by specific bacteriophages. Applied Microbiology 27: 251258.Google Scholar
Eklund, MW, Poysky, FT, Reed, SM and Smith, CA (1971). Bacteriophage and the toxigenicity of Clostridium botulinum type C. Science 172: 480482.CrossRefGoogle ScholarPubMed
Eklund, MW, Poysky, FT, Meyers, JA and Pelroy, GA (1974). Interspecies conversion of Clostridium botulinum type C to Clostridium novyi type A by bacteriophage. Science 186: 456458.Google Scholar
Elmund, GK, Morrison, SM, Grant, DW and Nevins, MP (1971). Role of excreted chlortetracycline in modifying the decomposition process in feedlot waste. Bulletin of Environmental Contamination and Toxicology 6: 129132.Google Scholar
Fajardo, A and Martínez, JL (2008). Antibiotics as signals that trigger specific bacterial responses. Current Opinion in Microbiology 11: 161167.Google Scholar
Feiner, R, Argov, T, Rabinovich, L, Sigal, N, Borovok, I and Herskovits, AA (2015). A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nature Reviews Microbiology 13: 641.Google Scholar
Figueroa-Bossi, N and Bossi, L (1999). Inducible prophages contribute to Salmonella virulence in mice. Molecular Microbiology 33: 167176.Google Scholar
Figueroa-Bossi, N, Uzzau, S, Maloriol, D and Bossi, L (2001). Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella. Molecular Microbiology 39: 260272.Google Scholar
Finley, RL, Collignon, P, Larsson, DJ, McEwen, SA, Li, X-Z, Gaze, WH, Reid-Smith, R, Timinouni, M, Graham, DW and Topp, E (2013). The scourge of antibiotic resistance: the important role of the environment. Clinical Infectious Diseases 57: 704710.Google Scholar
Flockhart, L, Pintar, K, Cook, A, McEwen, S, Friendship, R, Kelton, D and Pollari, F (2017). Distribution of Salmonella in humans, production animal operations and a watershed in a FoodNet Canada sentinel site. Zoonoses and Public Health 64: 4152.Google Scholar
Food and Drug Administration (2016). 2015 Summary Report on Antimicrobials Sold or Distributed for use in Food-Producing Animals. Rockville, MD: FDA. [Available online at https://www.fda.gov/downloads/ForIndustry/UserFees/AnimalDrugUserFeeActADUFA/UCM534243.pdf] [Accessed 24 July 2017].Google Scholar
Founou, LL, Founou, RC and Essack, SY (2016). Antibiotic resistance in the food chain: a developing country-perspective. Frontiers in Microbiology 7: 1881.Google Scholar
Frost, LS, Leplae, R, Summers, AO and Toussaint, A (2005). Mobile genetic elements: the agents of open source evolution. Nature Reviews Microbiology 3: 722.CrossRefGoogle ScholarPubMed
Giguère, S, Prescott, JF and Dowling, PM (2013). Antimicrobial Therapy in Veterinary Medicine. 5th edn. Ames, IA: Wiley-Blackwell, pp. 495518.CrossRefGoogle Scholar
Gustafson, RH and Kiser, JS (2012). Nonmedical uses of the tetracyclines. In: Hlavka, JJ and Boothe, JH (eds) The Tetracyclines. New York: Springer Science, pp. 405–349.Google Scholar
Huang, R, Ding, P, Huang, D and Yang, F (2015). Antibiotic pollution threatens public health in China. The Lancet 385: 773774.Google Scholar
Huss, HH (1980). Distribution of Clostridium botulinum. Applied and Environmental Microbiology 39: 764769.Google Scholar
Johnston, C, Martin, B, Fichant, G, Polard, P and Claverys, JP (2014). Bacterial transformation: distribution, shared mechanisms and divergent control. Nature Reviews Microbiology 12: 181196.Google Scholar
Kim, J-C, Chui, L, Wang, Y, Shen, J and Jeon, B (2016). Expansion of Shiga toxin-producing Escherichia coli by use of bovine antibiotic growth promoters. Emerging Infectious Diseases 22: 802.Google Scholar
Kirk, MD, Pires, SM, Black, RE, Caipo, M, Crump, JA, Devleesschauwer, B, Döpfer, D, Fazil, A, Fischer-Walker, CL, Hald, T and Hall, AJ (2015). World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis. PLoS Medicine 12: e1001921.CrossRefGoogle ScholarPubMed
Klare, I, Badstübner, D, Konstabel, C, Böhme, G, Claus, H and Witte, W (1999). Decreased incidence of VanA-type vancomycin-resistant enterococci isolated from poultry meat and from fecal samples of humans in the community after discontinuation of avoparcin usage in animal husbandry. Microbial Drug Resistance 5: 4552.Google Scholar
Koraimann, G and Wagner, MA (2014). Social behavior and decision making in bacterial conjugation. Frontiers in Cellular and Infection Microbiology 4: 54.Google Scholar
Li, Y-X, Zhang, X-L, Li, W, Lu, X-F, Liu, B and Wang, J (2013). The residues and environmental risks of multiple veterinary antibiotics in animal faeces. Environmental Monitoring and Assessment 185: 22112220.CrossRefGoogle ScholarPubMed
Lindsay, JA, Ruzin, A, Ross, HF, Kurepina, N and Novick, RP (1998). The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Molecular Microbiology 29: 527543.Google Scholar
Liu, L, Chen, X, Skogerbø, G, Zhang, P, Chen, R, He, S and Huang, DW (2012). The human microbiome: a hot spot of microbial horizontal gene transfer. Genomics 100: 265270.Google Scholar
Łoś, JM, Łoś, M and Węgrzyn, G (2011). Bacteriophages carrying Shiga toxin genes: genomic variations, detection and potential treatment of pathogenic bacteria. Future Microbiology 6: 909924.Google Scholar
Maiques, E, Úbeda, C, Campoy, S, Salvador, N, Lasa, Í, Novick, RP, Barbé, J and Penadés, JR (2006). β-Lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. Journal of Bacteriology 188: 27262729.Google Scholar
McGannon, CM, Fuller, CA and Weiss, AA (2010). Different classes of antibiotics differentially influence Shiga toxin production. Antimicrobial Agents and Chemotherapy 54: 37903798.CrossRefGoogle ScholarPubMed
Michel, B (2005). After 30 years of study, the bacterial SOS response still surprises us. PLoS Biology 3: e255.Google Scholar
Mirold, S, Rabsch, W, Rohde, M, Stender, S, Tschäpe, H, Rüssmann, H, Igwe, E and Hardt, WD (1999). Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proceedings of the National Academy of Sciences 96: 98459850.Google Scholar
Moon, BY, Park, JY, Hwang, SY, Robinson, DA, Thomas, JC, Fitzgerald, JR, Park, YH and Seo, KS (2015). Phage-mediated horizontal transfer of a Staphylococcus aureus virulence-associated genomic island. Scientific Reports 5.Google Scholar
Moore, P, Evenson, A, Luckey, T, McCoy, E, Elvehjem, C and Hart, E (1946). Use of sulfasuxidine, streptothricin, and streptomycin in nutritional studies with the chick. Journal of Biological Chemistry 165: 437441.Google Scholar
Myllykoski, J, Nevas, M, Lindström, M and Korkeala, H (2006). The detection and prevalence of Clostridium botulinum in pig intestinal samples. International Journal of Food Microbiology 110: 172177.Google Scholar
Nagaraja, T and Chengappa, M (1998). Liver abscesses in feedlot cattle: a review. Journal of Animal Science 76: 287298.Google Scholar
O'Connor, AM, Ziebell, KA, Poppe, C and McEwen, SA (2004). Verotoxins in commensal Escherichia coli in cattle: the effect of injectable subcutaneous oxytetracycline in addition to in-feed chlortetracycline on prevalence. Epidemiology and Infection 132: 7785.CrossRefGoogle ScholarPubMed
Pruden, A, Larsson, DJ, Amézquita, A, Collignon, P, Brandt, KK, Graham, DW, Lazorchak, JM, Suzuki, S, Silley, P, Snape, JR and Topp, E (2013). Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environmental Health Perspectives 121: 878.CrossRefGoogle ScholarPubMed
Pruimboom-Brees, IM, Morgan, TW, Ackermann, MR, Nystrom, ED, Samuel, JE, Cornick, NA and Moon, HW (2000). Cattle lack vascular receptors for Escherichia coli O157: H7 Shiga toxins. Proceedings of the National Academy of Sciences 97: 1032510329.Google Scholar
Ray, AJ, Pultz, NJ, Bhalla, A, Aron, DC and Donskey, CJ (2003). Coexistence of vancomycin-resistant enterococci and Staphylococcus aureus in the intestinal tracts of hospitalized patients. Clinical Infectious Diseases 37: 875881.Google Scholar
Salmond, GP and Fineran, PC (2015). A century of the phage: past, present and future. Nature Reviews Microbiology 13: 777786.Google Scholar
Sengeløv, G, Agersø, Y, Halling-Sørensen, B, Baloda, SB, Andersen, JS and Jensen, LB (2003). Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry. Environment International 28: 587595.CrossRefGoogle ScholarPubMed
Touchon, M, de Sousa, JA and Rocha, EP (2017). Embracing the enemy: the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer. Current Opinion in Microbiology 38: 6673.Google Scholar
Úbeda, C, Maiques, E, Knecht, E, Lasa, Í, Novick, RP and Penadés, JR (2005). Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Molecular Microbiology 56: 836844.Google Scholar
United States Department of Agriculture (2013). Feedlot 2011 part IV: health and health management on U.S. feedlots with a capacity of 1,000 or more head. USDA. [https://www.aphis.usda.gov/animal_health/nahms/feedlot/downloads/feedlot2011/Feed11_dr_PartIV.pdf ] [Accessed July 24 2017].Google Scholar
Van Boeckel, TP, Brower, C, Gilbert, M, Grenfell, BT, Levin, SA, Robinson, TP, Teillant, A and Laxminarayan, R (2015). Global trends in antimicrobial use in food animals. Proceedings of the National Academy of Sciences 112: 56495654.Google Scholar
Wagner, PL and Waldor, MK (2002). Bacteriophage control of bacterial virulence. Infection and Immunity 70: 39853993.Google Scholar
Weese, JS (2010). Methicillin-resistant Staphylococcus aureus in animals. ILAR Journal 51: 233244.Google Scholar
Wegener, HC (2003). Antibiotics in animal feed and their role in resistance development. Current Opinion in Microbiology 6: 439445.CrossRefGoogle ScholarPubMed
Yamaguchi, T, Hayashi, T, Takami, H, Nakasone, K, Ohnishi, M, Nakayama, K, Yamada, S, Komatsuzawa, H and Sugai, M (2000). Phage conversion of exfoliative toxin A production in Staphylococcus aureus. Molecular Microbiology 38: 694705.Google Scholar
Yamakawa, K, Kamiya, S, Yoshimura, K and Nakamura, S (1992). Clostridium botulinum type C in healthy swine in Japan. Microbiology and Immunology 36: 2934.Google Scholar
You, Y and Silbergeld, EK (2014). Learning from agriculture: understanding low-dose antimicrobials as drivers of resistome expansion. Frontiers in Microbiology 5.Google ScholarPubMed
Youngquist, CP, Mitchell, SM and Cogger, CG (2016). Fate of antibiotics and antibiotic resistance during digestion and composting: a review. Journal of Environmental Quality 45: 537545.Google Scholar
Yue, WF, Du, M and Zhu, MJ (2012). High temperature in combination with UV irradiation enhances horizontal transfer of stx2 gene from E. coli O157: H7 to non-pathogenic E. coli. PLoS ONE 7: e31308.Google Scholar
Zhang, QQ, Ying, GG, Pan, CG, Liu, YS and Zhao, JL (2015). Comprehensive evaluation of antibiotics emission and fate in the river basins of China: source analysis, multimedia modeling, and linkage to bacterial resistance. Environmental Science and Technology 11: 67726782.Google Scholar
Zhang, X, McDaniel, AD, Wolf, LE, Keusch, GT, Waldor, MK and Acheson, DW (2000). Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in mice. The Journal of Infectious Diseases 81: 664760.Google Scholar