Skip to main content
SpringerLink
Log in

Implications of bacteriophages on the acquisition and spread of antibiotic resistance in the environment

  • Review
  • Published:
International Microbiology Aims and scope Submit manuscript

Abstract

Although bacteriophages (or simply phages) are the most abundant biological entities and have the potential to transfer genetic material between bacterial hosts, their contribution to the acquisition and spread of antibiotic resistance genes in the environment has not been extensively studied. The environment is continually exposed to a wide variety of pollutants from anthropogenic sources, which may promote horizontal gene transfer events, including those mediated by phages. Considering the significant and growing concern of antibiotic resistance, phages should be taken into consideration during the implementation of mitigation measures. This review is focused on the emergence and spread of antibiotic resistance in the environment, with a special emphasis on the role of phages.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abeles SR, Ly M, Santiago-Rodriguez TM, Pride DT (2015) Effects of long term antibiotic therapy on human oral and fecal viromes. PLoS One 10:e0134941

    Article  Google Scholar 

  • Anand T, Bera BC, Vaid RK, Barua S, Riyesh T, Virmani N, Hussain M, Singh RK, Tripathi BN (2016) Abundance of antibiotic resistance genes in environmental bacteriophages. J Gen Virol 97:3458–3466

    Article  CAS  Google Scholar 

  • Caflisch KM, Patel R (2019) Implications of bacteriophage- and bacteriophage component-based therapies for the clinical microbiology laboratory. J Clin Microbiol 57:e00229–e00219

    Article  CAS  Google Scholar 

  • Calero-Cáceres W, Balcázar JL (2019) Antibiotic resistance genes in bacteriophages from diverse marine habitats. Sci Total Environ 654:452–455

    Article  Google Scholar 

  • Calero-Cáceres W, Muniesa M (2016) Persistence of naturally occurring antibiotic resistance genes in the bacteria and bacteriophage fractions of wastewater. Water Res 95:11–18

    Article  Google Scholar 

  • Calero-Cáceres W, Ye M, Balcázar JL (2019) Bacteriophages as environmental reservoirs of antibiotic resistance. Trends Microbiol 27:570–777

    Article  Google Scholar 

  • Callanan J, Stockdale SR, Shkoporov A, Draper LA, Ross RP, Hill C (2018) RNA phage biology in a metagenomic era. Viruses 10:386

    Article  Google Scholar 

  • Chen J, Quiles-Puchalt N, Chiang YN, Bacigalupe R, Fillol-Salom A, Chee MSJ, Fitzgerald JR, Penadés JR (2018) Genome hypermobility by lateral transduction. Science 362:207–212

    Article  CAS  Google Scholar 

  • Colomer-Lluch M, Jofre J, Muniesa M (2011) Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS One 6:e17549

    Article  CAS  Google Scholar 

  • Debroas D, Siguret C (2019) Viruses as key reservoirs of antibiotic resistance genes in the environment. ISME J 13:2856–2867

    Article  CAS  Google Scholar 

  • Enault F, Briet A, Bouteille L, Roux S, Sullivan MB, Petit MA (2017) Phages rarely encode antibiotic resistance genes: a cautionary tale for virome analyses. ISME J 11:237–247

    Article  CAS  Google Scholar 

  • Gandra S, Barter DM, Laxminarayan R (2014) Economic burden of antibiotic resistance: how much do we really know? Clin Microbiol Infect 20:973–980

    Article  CAS  Google Scholar 

  • Hatfull GF (2015) Dark matter of the biosphere: the amazing world of bacteriophage diversity. J Virol 89:8107–8110

    Article  CAS  Google Scholar 

  • Hilbert M, Csadek I, Auer U, Hilbert F (2017) Antimicrobial resistance-transducing bacteriophages isolated from surfaces of equine surgery clinics-a pilot study. Eur J Microbiol Immunol 7:296–302

    Article  CAS  Google Scholar 

  • Jiang SC, Paul JH (1998) Gene transfer by transduction in the marine environment. Appl Environ Microbiol 64:2780–2787

    Article  CAS  Google Scholar 

  • Kenzaka T, Tani K, Nasu M (2010) High-frequency phage-mediated gene transfer in freshwater environments determined at single-cell level. ISME J 4:648–659

    Article  CAS  Google Scholar 

  • Koskella B, Meaden S (2013) Understanding bacteriophage specificity in natural microbial communities. Viruses 5:806–823

    Article  Google Scholar 

  • Lekunberri I, Subirats J, Borrego CM, Balcázar JL (2017a) Exploring the contribution of bacteriophages to antibiotic resistance. Environ Pollut 220:981–984

    Article  CAS  Google Scholar 

  • Lekunberri I, Villagrasa M, Balcázar JL, Borrego CM (2017b) Contribution of bacteriophage and plasmid DNA to the mobilization of antibiotic resistance genes in a river receiving treated wastewater discharges. Sci Total Environ 601–602:206–209

    Article  Google Scholar 

  • Livermore DM, Blaser M, Carrs O, Cassell G, Fishman N, Guidos R, Levy S, Powers J, Norrby R, Tillotson G, Davies R, Projan S, Dawson A, Monnet D, Keogh-Brown M, Hand K, Garner S, Findlay D, Morel C, Wise R, Bax R, Burke F, Chopra I, Czaplewski L, Finch R, Piddock LJV, White T (2011) Discovery research: the scientific challenge of finding new antibiotics. J Antimicrob Chemother 66:1941–1944

    Article  CAS  Google Scholar 

  • Marti E, Variatza E, Balcázar JL (2014a) The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends Microbiol 22:36–41

    Article  CAS  Google Scholar 

  • Marti E, Variatza E, Balcázar JL (2014b) Bacteriophages as a reservoir of extended-spectrum β-lactamase and fluoroquinolone resistance genes in the environment. Clin Microbiol Infect 20:O456–O459

    Article  CAS  Google Scholar 

  • Modi SR, Lee HH, Spina CS, Collins JJ (2013) Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499:219–222

    Article  CAS  Google Scholar 

  • Novick R (1967) Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology 33:155–166

    Article  CAS  Google Scholar 

  • Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy MC, Michael I, Fatta-Kassinos D (2013) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447:345–360

    Article  CAS  Google Scholar 

  • Rolain JM, Abat C, Jimeno MT, Fournier PE, Raoult D (2016) Do we need new antibiotics? Clin Microbiol Infect 22:408–415

    Article  Google Scholar 

  • Roshini J, Raj M, Karunasagar I (2017) Prevalence of blaCTX-M-15 in coliphages isolated from sewage. Adv Sci Lett 23:1869–1871

    Article  Google Scholar 

  • Ross J, Topp E (2015) Abundance of antibiotic resistance genes in bacteriophage following soil fertilization with dairy manure or municipal biosolids, and evidence for potential transduction. Appl Environ Microbiol 81:7905–7913

    Article  CAS  Google Scholar 

  • Shousha A, Awaiwanont N, Sofka D, Smulders FJ, Paulsen P, Szostak MP, Humphrey T, Hilbert F (2015) Bacteriophages isolated from chicken meat and the horizontal transfer of antimicrobial resistance genes. Appl Environ Microbiol 81:4600–4606

    Article  CAS  Google Scholar 

  • Shrestha P, Cooper BS, Coast J, Oppong R, Do Thi Thuy N, Phodha T, Celhay O, Guerin PJ, Wertheim H, Lubell Y (2018) Enumerating the economic cost of antimicrobial resistance per antibiotic consumed to inform the evaluation of interventions affecting their use. Antimicrob Resist Infect Control 7:98

    Article  Google Scholar 

  • Singer AC, Shaw H, Rhodes V, Hart A (2016) Review of antimicrobial resistance in the environment and its relevance to environmental regulators. Front Microbiol 7:1728

    Article  Google Scholar 

  • Smith HW (1972) Ampicillin resistance in Escherichia coli by phage infection. Nat New Biol 238:205–206

    Article  CAS  Google Scholar 

  • Torres-Barceló C (2018) The disparate effects of bacteriophages on antibiotic-resistant bacteria. Emerg Microbes Infect 7:168

    Article  Google Scholar 

  • Wang M, Xiong W, Liu P, Xie X, Zeng J, Sun Y, Zeng Z (2018a) Metagenomic insights into the contribution of phages to antibiotic resistance in water samples related to swine feedlot wastewater treatment. Front Microbiol 9:2474

    Article  CAS  Google Scholar 

  • Wang M, Liu P, Zhou Q, Tao W, Sun Y, Zeng Z (2018b) Estimating the contribution of bacteriophage to the dissemination of antibiotic resistance genes in pig feces. Environ Pollut 238:291–298

    Article  CAS  Google Scholar 

  • Ye M, Sun M, Huang D, Zhang Z, Zhang H, Zhang S, Hu F, Jiang X, Jiao W (2019) A review of bacteriophage therapy for pathogenic bacteria inactivation in the soil environment. Environ Int 129:488–496

    Article  CAS  Google Scholar 

  • Zhang A, Call DR, Besser TE, Liu J, Jones L, Wang H, Davis MA (2019) β-lactam resistance genes in bacteriophage and bacterial DNA from wastewater, river water, and irrigation water in Washington State. Water Res 161:335–340

    Article  CAS  Google Scholar 

  • Zinder ND, Lederberg J (1952) Genetic exchange in Salmonella. J Bacteriol 64:679–699

    Article  CAS  Google Scholar 

Download references

Acknowledgments

I thank the Spanish Society for Microbiology (SEM) for honoring me with the Jaime Ferran Award 2019.

Funding

This work was supported by the Economy and Knowledge Department of the Catalan Government through Consolidated Research Group (ICRA-ENV 2017 SGR 1124).

Author information

Authors and Affiliations

  1. Catalan Institute for Water Research (ICRA), 17003, Girona, Spain

    José Luis Balcázar

  2. University of Girona, 17004, Girona, Spain

    José Luis Balcázar

Authors
  1. José Luis Balcázar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José Luis Balcázar.

Ethics declarations

Conflict of interest

The author declares that he has no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Balcázar, J.L. Implications of bacteriophages on the acquisition and spread of antibiotic resistance in the environment. Int Microbiol 23, 475–479 (2020). https://doi.org/10.1007/s10123-020-00121-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10123-020-00121-5

Keywords

Search

Navigation