Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Genomic surveillance for antimicrobial resistance — a One Health perspective

Abstract

Antimicrobial resistance (AMR) — the ability of microorganisms to adapt and survive under diverse chemical selection pressures — is influenced by complex interactions between humans, companion and food-producing animals, wildlife, insects and the environment. To understand and manage the threat posed to health (human, animal, plant and environmental) and security (food and water security and biosecurity), a multifaceted ‘One Health’ approach to AMR surveillance is required. Genomic technologies have enabled monitoring of the mobilization, persistence and abundance of AMR genes and mutations within and between microbial populations. Their adoption has also allowed source-tracing of AMR pathogens and modelling of AMR evolution and transmission. Here, we highlight recent advances in genomic AMR surveillance and the relative strengths of different technologies for AMR surveillance and research. We showcase recent insights derived from One Health genomic surveillance and consider the challenges to broader adoption both in developed and in lower- and middle-income countries.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Development of antimicrobial resistance.
Fig. 2: One Health antimicrobial resistance.
Fig. 3: One Health genomics toolbox.
Fig. 4: Plasmids as mobile genetic elements that drive antimicrobial resistance.

Similar content being viewed by others

References

  1. Djordjevic, S. P., Stokes, H. W. & Chowdhury, P. R. Mobile elements, zoonotic pathogens and commensal bacteria: conduits for the delivery of resistance genes into humans, production animals and soil microbiota. Front. Microbiol. 4, 86 (2013). This study addresses the importance of understanding how resistance genes and the genetic scaffolds that mobilize them into clinically important bacteria are likely to have their origins in completely unrelated parts of the microbial biosphere.

    Article  PubMed Central  PubMed  Google Scholar 

  2. Partridge, S. R., Kwong, S. M., Firth, N. & Jensen, S. O. Mobile genetic elements associated with antimicrobial resistance. Clin. Microbiol. Rev. 31, 00088 (2018). This study identifies the discerning features of MGEs that have the ability to move ARG cargo within or between DNA molecules and those that drive dissemination between bacterial cells.

    Article  Google Scholar 

  3. Gillings, M. R. Lateral gene transfer, bacterial genome evolution, and the Anthropocene. Ann. N. Y. Acad. Sci. 1389, 20–36 (2017).

    Article  PubMed  Google Scholar 

  4. Christaki, E., Marcou, M. & Tofarides, A. Antimicrobial resistance in bacteria: mechanisms, evolution, and persistence. J. Mol. Evol. 88, 26–40 (2020).

    Article  CAS  PubMed  Google Scholar 

  5. Aronin, S. I., Dunne, M. W., Yu, K. C., Watts, J. A. & Gupta, V. Increased rates of extended-spectrum β-lactamase isolates in patients hospitalized with culture-positive urinary Enterobacterales in the United States: 2011–2020. Diagn. Microbiol. Infect. Dis. 103, 115717 (2022).

    Article  CAS  PubMed  Google Scholar 

  6. Dejonckheere, Y., Desmet, S. & Knops, N. A study of the 20-year evolution of antimicrobial resistance patterns of pediatric urinary tract infections in a single center. Eur. J. Pediatr. https://doi.org/10.1007/s00431-022-04538-0 (2022). This study traces the evolution of drug resistance in paediatric patients with UTIs over a considerable time period.

    Article  PubMed  Google Scholar 

  7. Pires, J., Huisman, J. S., Bonhoeffer, S. & Van Boeckel, T. P. Increase in antimicrobial resistance in Escherichia coli in food animals between 1980 and 2018 assessed using genomes from public databases. J. Antimicrob. Chemother. 77, 646–655 (2022).

    Article  CAS  PubMed  Google Scholar 

  8. Schar, D. et al. Twenty-year trends in antimicrobial resistance from aquaculture and fisheries in Asia. Nat. Commun. 12, 5384 (2021). This large meta-analysis reports antibiotic-resistant bacteria from aquatic food animals in Asia from 2000 and highlights the need to study resistance to medically important antimicrobials in foodborne pathogens.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Turnidge, J. D., Meleady, K. T., Turnidge, J. D. & Meleady, K. T. Antimicrobial Use and Resistance in Australia (AURA) surveillance system: coordinating national data on antimicrobial use and resistance for Australia. Aust. Health Rev. 42, 272–276 (2017).

    Article  Google Scholar 

  10. Wyrsch, E. R. et al. Urban wildlife crisis: Australian silver gull is a bystander host to widespread clinical antibiotic resistance. mSystems 7, e0015822 (2022). This comprehensive WGS study of E. coli from an urban-adapted bird species highlights carriage of emerging and novel multiple drug-resistant lineages carrying genes encoding resistance to clinically important antibiotics.

    Article  PubMed  Google Scholar 

  11. Medvecky, M. et al. Interspecies transmission of CMY-2-producing Escherichia coli sequence type 963 isolates between humans and gulls in Australia. mSphere 7, e00238-22 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  12. Cummins, M. L., Reid, C. J. & Djordjevic, S. P. F Plasmid lineages in Escherichia coli ST95: implications for host range, antibiotic resistance, and zoonoses. mSystems 7, e01212–e01221 (2022). This study performs a phylogenomic analysis of ST95 and identifies lineages that carry different F virulence plasmids with implications for host colonization and zoonosis.

    CAS  PubMed Central  PubMed  Google Scholar 

  13. Inda-Díaz, J. S. et al. Latent antibiotic resistance genes are abundant, diverse, and mobile in human, animal, and environmental microbiomes. Microbiome 11, 44 (2023). This work highlights knowledge gaps in defining the resistome and describes the creation of a reference database for existing and latent antimicrobial resistance genes.

    Article  PubMed Central  PubMed  Google Scholar 

  14. Baker, S., Thomson, N., Weill, F.-X. & Holt, K. E. Genomic insights into the emergence and spread of antimicrobial-resistant bacterial pathogens. Science 360, 733–738 (2018).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Lane, C. R. et al. Search and contain: impact of an integrated genomic and epidemiological surveillance and response program for control of carbapenemase-producing Enterobacterales. Clin. Infect. Dis. 73, e3912–e3920 (2021).

    Article  CAS  PubMed  Google Scholar 

  16. Sia, C. M. et al. Genomic diversity of antimicrobial resistance in non-typhoidal Salmonella in Victoria, Australia. Microb. Genom. 7, 000725 (2021).

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Bharat, A. et al. Correlation between phenotypic and in silico detection of antimicrobial resistance in Salmonella enterica in Canada using Staramr. Microorganisms 10, 292 (2022).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Rebelo, A. R. et al. One day in Denmark: comparison of phenotypic and genotypic antimicrobial susceptibility testing in bacterial isolates from clinical settings. Front. Microbiol. 13, 804627 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  19. Sherry, N. L. et al. An ISO-certified genomics workflow for identification and surveillance of antimicrobial resistance. Nat. Commun. 14, 60 (2023). This paper is one of the first to demonstrate the certification of genomic interpretation of AMR to ISO standards, providing a framework for implementation into public health surveillance.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Hendriksen, R. S. et al. Using genomics to track global antimicrobial resistance. Front. Public Health 7, 00242 (2019).

    Article  Google Scholar 

  21. Papp, M. & Solymosi, N. Review and comparison of antimicrobial resistance gene databases. Antibiotics 11, 339 (2022).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Kim, J. I. et al. Machine learning for antimicrobial resistance prediction: current practice, limitations, and clinical perspective. Clin. Microbiol. Rev. 35, e00179-21 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  23. Meyer, F. et al. Critical assessment of metagenome interpretation: the second round of challenges. Nat. Methods 19, 429–440 (2022).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. DeMaere, M. Z. & Darling, A. E. bin3C: exploiting Hi-C sequencing data to accurately resolve metagenome-assembled genomes. Genome Biol. 20, 46 (2019).

    Article  PubMed Central  PubMed  Google Scholar 

  25. Zankari, E. et al. PointFinder: a novel web tool for WGS-based detection of antimicrobial resistance associated with chromosomal point mutations in bacterial pathogens. J. Antimicrob. Chemother. 72, 2764–2768 (2017).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Zankari, E. et al. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67, 2640–2644 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. McArthur, A. G. et al. The Comprehensive Antibiotic Resistance Database. Antimicrob. Agents Chemother. 57, 3348–3357 (2013).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Feldgarden, M. et al. Curation of the AMRFinderPlus databases: applications, functionality and impact. Microb. Genom. 8, mgen000832 (2022).

    PubMed Central  PubMed  Google Scholar 

  29. Arango-Argoty, G. A. et al. ARGminer: a web platform for the crowdsourcing-based curation of antibiotic resistance genes. Bioinformatics 36, 2966–2973 (2020).

    Article  CAS  PubMed  Google Scholar 

  30. Gibson, M. K., Forsberg, K. J. & Dantas, G. Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. ISME J. 9, 207–216 (2015).

    Article  CAS  PubMed  Google Scholar 

  31. Hunt, M. et al. ARIBA: rapid antimicrobial resistance genotyping directly from sequencing reads. Micro. Genom. 3, e000131 (2017).

    Google Scholar 

  32. Clausen, P. T. L. C., Aarestrup, F. M. & Lund, O. Rapid and precise alignment of raw reads against redundant databases with KMA. BMC Bioinforma. 19, 307 (2018).

    Article  Google Scholar 

  33. Steinig, E. et al. Phylodynamic signatures in the emergence of community-associated MRSA. Proc. Natl Acad. Sci. USA 119, e2204993119 (2022).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Steinig, E. et al. Phylodynamic inference of bacterial outbreak parameters using nanopore sequencing. Mol. Biol. Evol. 39, msac040 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  35. Rife, B. D. et al. Phylodynamic applications in 21st century global infectious disease research. Glob. Health Res. Policy 2, 13 (2017).

    Article  PubMed Central  PubMed  Google Scholar 

  36. Dawson, D., Rasmussen, D., Peng, X. & Lanzas, C. Inferring environmental transmission using phylodynamics: a case-study using simulated evolution of an enteric pathogen. J. R. Soc. Interface 18, 20210041 (2021).

    Article  PubMed Central  PubMed  Google Scholar 

  37. Ingle, D. J., Howden, B. P. & Duchene, S. Development of phylodynamic methods for bacterial pathogens. Trends Microbiol. 29, 788–797 (2021). This important review highlights the potential utility of phylodynamic analyses to enhance understanding of bacterial evolution and transmission.

    Article  CAS  PubMed  Google Scholar 

  38. Miłobedzka, A. et al. Monitoring antibiotic resistance genes in wastewater environments: the challenges of filling a gap in the One-Health cycle. J. Hazard. Mater. 424, 127407 (2022).

    Article  PubMed  Google Scholar 

  39. Munk, P. et al. Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance. Nat. Commun. 13, 7251 (2022).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Liguori, K. et al. Antimicrobial resistance monitoring of water environments: a framework for standardized methods and quality control. Environ. Sci. Technol. 56, 9149–9160 (2022). This work presents a framework developed in consultation with experts in academia, government and water utility management, and through analyses of the literature, describes standardized methods for monitoring AMR in water.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Hendriksen, R. S. et al. Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage. Nat. Commun. 10, 1124 (2019). This work presents metagenomic sequencing of sewage as an economically and ethically acceptable approach to global AMR surveillance, providing important insights into AMR carriage in the healthy human gut in a region-specific manner.

    Article  PubMed Central  PubMed  Google Scholar 

  42. Banerjee, S. & van der Heijden, M. G. A. Soil microbiomes and one health. Nat. Rev. Microbiol. 21, 6–20 (2023).

    Article  CAS  PubMed  Google Scholar 

  43. Larsson, D. G. J. & Flach, C.-F. Antibiotic resistance in the environment. Nat. Rev. Microbiol. 20, 257–269 (2022). This review examines risk scenarios, surveillance methods and potential factors driving antibiotic resistance, and identifies actionable measures to mitigate the risks associated with antibiotic resistance in the environment.

    Article  CAS  PubMed  Google Scholar 

  44. Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet 399, 629–655 (2022).

    Article  Google Scholar 

  45. Kim, D.-W. & Cha, C.-J. Antibiotic resistome from the One-Health perspective: understanding and controlling antimicrobial resistance transmission. Exp. Mol. Med. 53, 301–309 (2021).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Lamberte, L. E. & van Schaik, W. Antibiotic resistance in the commensal human gut microbiota. Curr. Opin. Microbiol. 68, 102150 (2022).

    Article  CAS  PubMed  Google Scholar 

  47. Crits-Christoph, A., Hallowell, H. A., Koutouvalis, K. & Suez, J. Good microbes, bad genes? The dissemination of antimicrobial resistance in the human microbiome. Gut Microbes 14, 2055944 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  48. Arumugam, K. et al. Recovery of complete genomes and non-chromosomal replicons from activated sludge enrichment microbial communities with long read metagenome sequencing. npj Biofilms Microbiomes 7, 1–13 (2021).

    Article  Google Scholar 

  49. Bertrand, D. et al. Hybrid metagenomic assembly enables high-resolution analysis of resistance determinants and mobile elements in human microbiomes. Nat. Biotechnol. 37, 937–944 (2019).

    Article  CAS  PubMed  Google Scholar 

  50. Kolmogorov, M. et al. metaFlye: scalable long-read metagenome assembly using repeat graphs. Nat. Methods 17, 1103–1110 (2020).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Pellow, D. et al. SCAPP: an algorithm for improved plasmid assembly in metagenomes. Microbiome 9, 144 (2021).

    Article  PubMed Central  PubMed  Google Scholar 

  52. Somerville, V. et al. Long-read based de novo assembly of low-complexity metagenome samples results in finished genomes and reveals insights into strain diversity and an active phage system. BMC Microbiol. 19, 143 (2019).

    Article  PubMed Central  PubMed  Google Scholar 

  53. Fitzpatrick, F., Doherty, A. & Lacey, G. Using artificial intelligence in infection prevention. Curr. Treat. Options Infect. Dis. 12, 135–144 (2020).

    Article  PubMed Central  PubMed  Google Scholar 

  54. Wheeler, N. E., Gardner, P. P. & Barquist, L. Machine learning identifies signatures of host adaptation in the bacterial pathogen Salmonella enterica. PLoS Genet. 14, e1007333 (2018).

    Article  PubMed Central  PubMed  Google Scholar 

  55. Lupolova, N., Dallman, T. J., Holden, N. J. & Gally, D. L. Patchy promiscuity: machine learning applied to predict the host specificity of Salmonella enterica and Escherichia coli. Microb. Genom. 3, e000135 (2017).

    PubMed Central  PubMed  Google Scholar 

  56. Munck, N., Njage, P. M. K., Leekitcharoenphon, P., Litrup, E. & Hald, T. Application of whole-genome sequences and machine learning in source attribution of Salmonella typhimurium. Risk Anal. 40, 1693–1705 (2020).

    Article  PubMed Central  PubMed  Google Scholar 

  57. Tanui, C. K., Benefo, E. O., Karanth, S. & Pradhan, A. K. A machine learning model for food source attribution of Listeria monocytogenes. Pathogens 11, 691 (2022).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  58. Li, L.-G., Yin, X. & Zhang, T. Tracking antibiotic resistance gene pollution from different sources using machine-learning classification. Microbiome 6, 93 (2018).

    Article  PubMed Central  PubMed  Google Scholar 

  59. Vassallo, A., Kett, S., Purchase, D. & Marvasi, M. Antibiotic-resistant genes and bacteria as evolving contaminants of emerging concerns (e-CEC): is it time to include evolution in risk assessment? Antibiotics 10, 1066 (2021).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Ikhimiukor, O. O., Odih, E. E., Donado-Godoy, P. & Okeke, I. N. A bottom-up view of antimicrobial resistance transmission in developing countries. Nat. Microbiol. 7, 757–765 (2022).

    Article  CAS  PubMed  Google Scholar 

  61. O’Neill, J. Antimicrobial resistance: tackling a crisis for the health and wealth of nations. Wellcome Collection https://wellcomecollection.org/works/rdpck35v/items (2014).

  62. Flowers, P. Antimicrobial resistance: a biopsychosocial problem requiring innovative interdisciplinary and imaginative interventions. J. Infect. Prev. 19, 195–199 (2018).

    Article  PubMed Central  PubMed  Google Scholar 

  63. Raboisson, D., Ferchiou, A., Sans, P., Lhermie, G. & Dervillé, M. The economics of antimicrobial resistance in veterinary medicine: optimizing societal benefits through mesoeconomic approaches from public and private perspectives. One Health 10, 100145 (2020).

    Article  PubMed Central  PubMed  Google Scholar 

  64. George, A. Antimicrobial resistance (AMR) in the food chain: trade, One Health and Codex. Trop. Med. Infect. Dis. 4, 54 (2019).

    Article  PubMed Central  PubMed  Google Scholar 

  65. Queenan, K., Häsler, B. & Rushton, J. A One Health approach to antimicrobial resistance surveillance: is there a business case for it? Int. J. Antimicrob. Agents 48, 422–427 (2016).

    Article  CAS  PubMed  Google Scholar 

  66. Collignon, P. J. & McEwen, S. A. One Health—its importance in helping to better control antimicrobial resistance. Trop. Med. Infect. Dis. 4, 22 (2019).

    Article  PubMed Central  PubMed  Google Scholar 

  67. McEwen, S. A. & Collignon, P. J. Antimicrobial resistance: a One Health perspective. Microbiol. Spectr. https://doi.org/10.1128/microbiolspec.arba-0009-2017 (2018).

    Article  PubMed  Google Scholar 

  68. World Health Organization. The fight against antimicrobial resistance is closely linked to the sustainable development goals. https://apps.who.int/iris/handle/10665/337519. (WHO, 2020).

  69. Sartelli, M. et al. Antibiotic use in low and middle-income countries and the challenges of antimicrobial resistance in surgery. Antibiotics 9, 497 (2020).

    Article  PubMed Central  PubMed  Google Scholar 

  70. Collignon, P., Athukorala, P., Senanayake, S. & Khan, F. Antimicrobial resistance: the major contribution of poor governance and corruption to this growing problem. PLoS ONE 10, e0116746 (2015).

    Article  PubMed Central  PubMed  Google Scholar 

  71. Harant, A. Assessing transparency and accountability of national action plans on antimicrobial resistance in 15 African countries. Antimicrob. Resist. Infect. Control 11, 15 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  72. Musoke, D. et al. The role of environmental health in preventing antimicrobial resistance in low- and middle-income countries. Environ. Health Prev. Med. 26, 100 (2021).

    Article  PubMed Central  PubMed  Google Scholar 

  73. Muloi, D. M. et al. Population genomics of Escherichia coli in livestock-keeping households across a rapidly developing urban landscape. Nat. Microbiol. 7, 581–589 (2022). This WGS analysis of E. coli from humans, livestock and wildlife across households in Nairobi, Kenya shows evidence of interhost and interhousehold transmission, with implications for the emergence of zoonoses and the spread of AMR.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Horrigan, L., Lawrence, R. S. & Walker, P. How sustainable agriculture can address the environmental and human health harms of industrial agriculture. Environ. Health Perspect. 110, 445–456 (2002).

    Article  PubMed Central  PubMed  Google Scholar 

  75. Sanz-García, F. et al. Translating eco-evolutionary biology into therapy to tackle antibiotic resistance. Nat. Rev. Microbiol. https://doi.org/10.1038/s41579-023-00902-5 (2023).

    Article  PubMed  Google Scholar 

  76. David, S. et al. Epidemic of carbapenem-resistant Klebsiella pneumoniae in Europe is driven by nosocomial spread. Nat. Microbiol. 4, 1919–1929 (2019).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  77. Denamur, E. et al. High frequency of mutator strains among human uropathogenic Escherichia coli isolates. J. Bacteriol. 184, 605–609 (2002).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Denamur, E. & Matic, I. Evolution of mutation rates in bacteria. Mol. Microbiol. 60, 820–827 (2006).

    Article  CAS  PubMed  Google Scholar 

  79. Reeves, P. R. et al. Rates of mutation and host transmission for an Escherichia coli clone over 3 years. PLoS ONE 6, e26907 (2011).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  80. Duval, A., Opatowski, L. & Brisse, S. Defining genomic epidemiology thresholds for common-source bacterial outbreaks: a modelling study. Lancet Microbe 4, e349–e357 (2023).

    Article  PubMed Central  PubMed  Google Scholar 

  81. Thorpe, H. A. et al. A large-scale genomic snapshot of Klebsiella spp. isolates in northern Italy reveals limited transmission between clinical and non-clinical settings. Nat. Microbiol. 7, 2054–2067 (2022).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  82. Rice, L. B. Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE. J. Infect. Dis. 197, 1079–1081 (2008).

    Article  PubMed  Google Scholar 

  83. Rice, L. B. Progress and challenges in implementing the research on ESKAPE pathogens. Infect. Control. Hosp. Epidemiol. 31 (Suppl. 1), S7–S10 (2010).

    Article  PubMed  Google Scholar 

  84. Boucher, H. W. et al. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin. Infect. Dis. 48, 1–12 (2009).

    Article  PubMed  Google Scholar 

  85. Pendleton, J. N., Gorman, S. P. & Gilmore, B. F. Clinical relevance of the ESKAPE pathogens. Expert. Rev. Anti Infect. Ther. 11, 297–308 (2013).

    Article  CAS  PubMed  Google Scholar 

  86. Diekema, D. J. et al. The microbiology of bloodstream infection: 20-year trends from the SENTRY antimicrobial surveillance program. Antimicrob. Agents Chemother. 63, e00355-19 (2019).

    Article  PubMed Central  PubMed  Google Scholar 

  87. Kajihara, T., Yahara, K., Hirabayashi, A., Shibayama, K. & Sugai, M. Japan Nosocomial Infections Surveillance (JANIS): current status, international collaboration, and future directions for a comprehensive antimicrobial resistance surveillance system. Jpn. J. Infect. Dis. 74, 87–96 (2021).

    Article  PubMed  Google Scholar 

  88. Wyres, K. L. & Holt, K. E. Klebsiella pneumoniae as a key trafficker of drug resistance genes from environmental to clinically important bacteria. Curr. Opin. Microbiol. 45, 131–139 (2018). This paper presents data to support the contention that Klebsiella spp. as a genus may play a seminal role in capturing and spreading AMR genes from environmental microbial populations into the ESKAPE and other clinically important pathogens.

    Article  CAS  PubMed  Google Scholar 

  89. von Wintersdorff, C. J. H. et al. Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer. Front. Microbiol. 7, 173 (2016).

    Google Scholar 

  90. O’Neal, L., Alvarez, D., Mendizábal-Cabrera, R., Ramay, B. M. & Graham, J. Community-acquired antimicrobial resistant Enterobacteriaceae in Central America: a One Health systematic review. Int. J. Environ. Res. Public Health 17, 7622 (2020).

    Article  PubMed Central  PubMed  Google Scholar 

  91. Campos-Madueno, E. I. et al. Carbapenemase-producing Klebsiella pneumoniae strains in Switzerland: human and non-human settings may share high-risk clones. J. Glob. Antimicrob. Resist. 28, 206–215 (2022).

    Article  CAS  PubMed  Google Scholar 

  92. D’Costa, V. M. et al. Antibiotic resistance is ancient. Nature 477, 457–461 (2011).

    Article  PubMed  Google Scholar 

  93. Poirel, L. et al. Identification of FosA8, a plasmid-encoded fosfomycin resistance determinant from Escherichia coli, and its origin in Leclercia adecarboxylata. Antimicrob. Agents Chemother. https://doi.org/10.1128/aac.01403-19 (2019).

    Article  PubMed Central  PubMed  Google Scholar 

  94. Poirel, L., Rodriguez-Martinez, J.-M., Mammeri, H., Liard, A. & Nordmann, P. Origin of plasmid-mediated quinolone resistance determinant QnrA. Antimicrob. Agents Chemother. 49, 3523–3525 (2005).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  95. Tacão, M., Araújo, S., Vendas, M., Alves, A. & Henriques, I. Shewanella species as the origin of blaOXA-48 genes: insights into gene diversity, associated phenotypes and possible transfer mechanisms. Int. J. Antimicrob. Agents 51, 340–348 (2018).

    Article  PubMed  Google Scholar 

  96. Canton, R., Gonzalez-Alba, J. M. & Galán, J. C. CTX-M enzymes: origin and diffusion. Front. Microbiol. 3, 110 (2012).

    Article  PubMed Central  PubMed  Google Scholar 

  97. Rodríguez, M. M. et al. Chromosome-encoded CTX-M-3 from Kluyvera ascorbata: a possible origin of plasmid-borne CTX-M-1-derived cefotaximases. Antimicrob. Agents Chemother. 48, 4895–4897 (2004).

    Article  PubMed Central  PubMed  Google Scholar 

  98. Sekizuka, T. et al. Complete sequencing of the blaNDM-1-positive IncA/C plasmid from Escherichia coli ST38 isolate suggests a possible origin from plant pathogens. PLoS ONE 6, e25334 (2011).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  99. Wang, R. et al. The global distribution and spread of the mobilized colistin resistance gene mcr-1. Nat. Commun. 9, 1179 (2018).

    Article  PubMed Central  PubMed  Google Scholar 

  100. Castillo-Ramírez, S. Zoonotic Acinetobacter baumannii: the need for genomic epidemiology in a One Health context. Lancet Microbe 3, e895–e896 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  101. Prity, F. T. et al. The evolutionary tale of eight novel plasmids in a colistin-resistant environmental Acinetobacter baumannii isolate. Microb. Genom. 9, mgen001010 (2023).

    PubMed Central  PubMed  Google Scholar 

  102. Liu, C. M. et al. Using source-associated mobile genetic elements to identify zoonotic extraintestinal E. coli infections. One Health https://doi.org/10.1016/j.onehlt.2023.100518 (2023). This large, geographically matched, comparative genomic analysis of contemporaneous clinical and meat-source E. coli isolates identifies source-associated MGEs and estimates that approximately 8% of human extraintestinal E. coli infections are potentially attributable to foodborne zoonotic E. coli.

    Article  PubMed Central  PubMed  Google Scholar 

  103. Matlock, W. et al. Enterobacterales plasmid sharing amongst human bloodstream infections, livestock, wastewater, and waterway niches in Oxfordshire, UK. eLife 12, e85302 (2023). This pan-genome analysis of plasmid clusters in a geographically and temporally selected subset of isolates shows evidence of widespread plasmid sharing across species and niches and accessory cargo exchange.

    Article  PubMed Central  PubMed  Google Scholar 

  104. Swarthout, J. M., Chan, E. M. G., Garcia, D., Nadimpalli, M. L. & Pickering, A. J. Human colonization with antibiotic-resistant bacteria from nonoccupational exposure to domesticated animals in low- and middle-income countries: a critical review. Environ. Sci. Technol. 56, 14875–14890 (2022).

    Article  CAS  PubMed  Google Scholar 

  105. Price, L. B., Hungate, B. A., Koch, B. J., Davis, G. S. & Liu, C. M. Colonizing opportunistic pathogens (COPs): the beasts in all of us. PLoS Pathog. 13, e1006369 (2017). E. coli (ExPEC), K. pneumoniae and Streptococcus pneumoniae are important examples of colonizing opportunistic pathogens with a benign existence in the human body, but when conditions favour their transition to a pathogenic state, often in a different body site, they exact a horrendous toll on human health.

    Article  PubMed Central  PubMed  Google Scholar 

  106. Castillo-Ramírez, S., Ghaly, T. & Gillings, M. Non-clinical settings—the understudied facet of antimicrobial drug resistance. Environ. Microbiol. 23, 7271–7274 (2021).

    Article  PubMed  Google Scholar 

  107. Montalbano Di Filippo, M. et al. Exploring the nature of interaction between shiga toxin producing Escherichia coli (STEC) and free-living amoeba—Acanthamoeba sp. Front. Cell. Infect. Microbiol. 12, 926127 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  108. Loest, D. et al. Carbapenem-resistant Escherichia coli from shrimp and salmon available for purchase by consumers in Canada: a risk profile using the Codex framework. Epidemiol. Infect. 150, e148 (2022).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  109. Zhang, Q. et al. Rapid increase in carbapenemase-producing Enterobacteriaceae in retail meat driven by the spread of the blaNDM-5-carrying IncX3 plasmid in China from 2016 to 2018. Antimicrob. Agents Chemother. 63, e00573-19 (2019).

    Article  PubMed Central  PubMed  Google Scholar 

  110. Jamin, C. et al. Genetic analysis of plasmid-encoded mcr-1 resistance in Enterobacteriaceae derived from poultry meat in the Netherlands. JAC Antimicrob. Resist. 3, dlab156 (2021).

    Article  PubMed Central  PubMed  Google Scholar 

  111. Feng, J. et al. Characterization of carbapenem-resistant enterobacteriaceae cultured from retail meat products, patients, and porcine excrement in China. Front. Microbiol. 12, 743468 (2021).

    Article  PubMed Central  PubMed  Google Scholar 

  112. Reid, C. J., Blau, K., Jechalke, S., Smalla, K. & Djordjevic, S. P. Whole genome sequencing of Escherichia coli from store-bought produce. Front. Microbiol. 10, 3050 (2020).

    Article  PubMed Central  PubMed  Google Scholar 

  113. Igbinosa, E. O., Beshiru, A., Igbinosa, I. H., Cho, G.-S. & Franz, C. M. A. P. Multidrug-resistant extended spectrum β-lactamase (ESBL)-producing Escherichia coli from farm produce and agricultural environments in Edo State, Nigeria. PLoS ONE 18, e0282835 (2023).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  114. Chelaghma, W. et al. Occurrence of extended spectrum cephalosporin-, carbapenem- and colistin-resistant Gram-negative bacteria in fresh vegetables, an increasing human health concern in Algeria. Antibiotics 11, 988 (2022).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  115. Manageiro, V., Jones-Dias, D., Ferreira, E. & Caniça, M. Plasmid-mediated colistin resistance (mcr-1) in Escherichia coli from non-imported fresh vegetables for human consumption in Portugal. Microorganisms 8, 429 (2020).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  116. Teng, L. et al. A cross-sectional study of companion animal-derived multidrug-resistant Escherichia coli in Hangzhou, China. Microbiol. Spectr. 11, e02113–e02122 (2023).

    Article  PubMed Central  PubMed  Google Scholar 

  117. Marques, C. et al. Increase in antimicrobial resistance and emergence of major international high-risk clonal lineages in dogs and cats with urinary tract infection: 16 year retrospective study. J. Antimicrob. Chemother. 73, 377–384 (2018).

    Article  CAS  PubMed  Google Scholar 

  118. Garcês, A. et al. Bacterial isolates from urinary tract infection in dogs and cats in Portugal, and their antibiotic susceptibility pattern: a retrospective study of 5 years (2017–2021). Antibiotics 11, 1520 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  119. Sano, E. et al. One Health clones of multidrug-resistant Escherichia coli carried by synanthropic animals in Brazil. One Health 16, 100476 (2023).

    Article  PubMed  Google Scholar 

  120. Devnath, P., Karah, N., Graham, J. P., Rose, E. S. & Asaduzzaman, M. Evidence of antimicrobial resistance in bats and its planetary health impact for surveillance of zoonotic spillover events: a scoping review. Int. J. Environ. Res. Public Health 20, 243 (2023).

    Article  CAS  Google Scholar 

  121. Martín-Maldonado, B. et al. Urban birds as antimicrobial resistance sentinels: white storks showed higher multidrug-resistant Escherichia coli levels than seagulls in Central Spain. Animals 12, 2714 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  122. Torres, R. T. et al. A walk on the wild side: wild ungulates as potential reservoirs of multi-drug resistant bacteria and genes, including Escherichia coli harbouring CTX-M β-lactamases. Environ. Pollut. 306, 119367 (2022).

    Article  CAS  PubMed  Google Scholar 

  123. Martinson, J. N. V. et al. Rethinking gut microbiome residency and the Enterobacteriaceae in healthy human adults. ISME J. 13, 2306–2318 (2019).

    Article  PubMed Central  PubMed  Google Scholar 

  124. Martinson, J. N. V. & Walk, S. T. Escherichia coli residency in the gut of healthy human adults. EcoSal 9, ESP0003 (2020).

    Google Scholar 

  125. Yu, D., Ryu, K., Zhi, S., Otto, S. J. G. & Neumann, N. F. Naturalized Escherichia coli in wastewater and the co-evolution of bacterial resistance to water treatment and antibiotics. Front. Microbiol. 13, 810312 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  126. Guragain, M., Brichta-Harhay, D. M., Bono, J. L. & Bosilevac, J. M. Locus of heat resistance (LHR) in meat-borne Escherichia coli: screening and genetic characterization. Appl. Environ. Microbiol. 87, e02343-20 (2021).

    Article  PubMed Central  PubMed  Google Scholar 

  127. Marin, J. et al. The population genomics of increased virulence and antibiotic resistance in human commensal Escherichia coli over 30 years in France. Appl. Environ. Microbiol. 88, e00664-22 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  128. Massot, M. et al. Phylogenetic, virulence and antibiotic resistance characteristics of commensal strain populations of Escherichia coli from community subjects in the Paris area in 2010 and evolution over 30 years. Microbiology 162, 642–650 (2016).

    Article  CAS  PubMed  Google Scholar 

  129. Flannery, D. D. et al. Antibiotic susceptibility of Escherichia coli among infants admitted to neonatal intensive care units across the US from 2009 to 2017. JAMA Pediatr. 175, 168–175 (2021).

    Article  PubMed  Google Scholar 

  130. Cassini, A. et al. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. Lancet Infect. Dis. 19, 56–66 (2019).

    Article  PubMed Central  PubMed  Google Scholar 

  131. Poolman, J. T. & Wacker, M. Extraintestinal pathogenic Escherichia coli, a common human pathogen: challenges for vaccine development and progress in the field. J. Infect. Dis. 213, 6–13 (2016).

    Article  CAS  PubMed  Google Scholar 

  132. Weiner-Lastinger, L. M. et al. Antimicrobial-resistant pathogens associated with adult healthcare-associated infections: summary of data reported to the National Healthcare Safety Network, 2015–2017. Infect. Control. Hospital Epidemiol. 41, 1–18 (2020).

    Article  Google Scholar 

  133. Foxman, B. Urinary tract infection syndromes: occurrence, recurrence, bacteriology, risk factors, and disease burden. Infect. Dis. Clin. North Am. 28, 1–13 (2014).

    Article  PubMed  Google Scholar 

  134. Tacconelli, E. et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect. Dis. 18, 318–327 (2018).

    Article  PubMed  Google Scholar 

  135. United Nations Environment Programme. Bracing for superbugs: strengthening environmental action in the One Health response to antimicrobial resistance https://www.unep.org/resources/superbugs/environmental-action (2023).

  136. World Health Organization. WHO integrated global surveillance on ESBL-producing E. coli using a “One Health” approach: implementation and opportunities. (WHO, 2021).

  137. Livermore, D. M. Defining an extended-spectrum β-lactamase. Clin. Microbiol. Infect. 14, 3–10 (2008).

    Article  CAS  PubMed  Google Scholar 

  138. Livermore, D. M. & Hawkey, P. M. CTX-M: changing the face of ESBLs in the UK. J. Antimicrob. Chemother. 56, 451–454 (2005).

    Article  CAS  PubMed  Google Scholar 

  139. Ludden, C. et al. Defining nosocomial transmission of Escherichia coli and antimicrobial resistance genes: a genomic surveillance study. Lancet Microbe 2, e472–e480 (2021).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  140. Manges, A. R. Escherichia coli causing bloodstream and other extraintestinal infections: tracking the next pandemic. Lancet Infect. Dis. 19, 1269–1270 (2019).

    Article  PubMed  Google Scholar 

  141. Mills, E. G. et al. A one-year genomic investigation of Escherichia coli epidemiology and nosocomial spread at a large US healthcare network. Genome Med. 14, 147 (2022).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  142. Stephens, C. M., Adams-Sapper, S., Sekhon, M., Johnson, J. R. & Riley, L. W. Genomic analysis of factors associated with low prevalence of antibiotic resistance in extraintestinal pathogenic Escherichia coli sequence type 95 strains. mSphere 2, e00390 (2017).

    Article  PubMed Central  PubMed  Google Scholar 

  143. Carrilero, L., Dunn, S. J., Moran, R. A., McNally, A. & Brockhurst, M. A. Evolutionary responses to acquiring a multidrug resistance plasmid are dominated by metabolic functions across diverse Escherichia coli lineages. mSystems 8, e0071322 (2023).

    Article  PubMed  Google Scholar 

  144. Reid, C. J. et al. A role for ColV plasmids in the evolution of pathogenic Escherichia coli ST58. Nat. Commun. 13, 1–15 (2022). This report explores important concepts that underpin the emergence of a pathogenic lineage of E. coli with emphasis on the role played by the stable co-acquisition of key virulence-associated genes.

    Article  Google Scholar 

  145. Li, L. et al. Genomic characterization of mcr-1-carrying foodborne Salmonella enterica serovar Typhimurium and identification of a transferable plasmid carrying mcr-1, blaCTX-M-14, qnrS2, and oqxAB genes from ready-to-eat pork product in China. Front. Microbiol. 13, 903268 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  146. Macori, G. et al. Characterisation of early positive mcr-1 resistance gene and plasmidome in Escherichia coli pathogenic strains associated with variable phylogroups under colistin selection. Antibiotics 10, 1041 (2021).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  147. Zhang, X. et al. Spread and molecular characteristics of enterobacteriaceae carrying fosA-like genes from farms in China. Microbiol. Spectr. 10, e005422 (2022).

    Google Scholar 

  148. Zhao, W.-H. & Hu, Z.-Q. Epidemiology and genetics of CTX-M extended-spectrum β-lactamases in Gram-negative bacteria. Crit. Rev. Microbiol. 39, 79–101 (2013).

    Article  CAS  PubMed  Google Scholar 

  149. Du, P. et al. Novel IS26-mediated hybrid plasmid harbouring tetX4 in Escherichia coli. J. Glob. Antimicrob. Resist. 21, 162–168 (2020).

    Article  PubMed  Google Scholar 

  150. He, D. et al. Emergence of a hybrid plasmid derived from IncN1-F33:A−:B− and mcr-1-bearing plasmids mediated by IS26. J. Antimicrob. Chemother. 74, 3184–3189 (2019).

    Article  CAS  PubMed  Google Scholar 

  151. Vinué, L. et al. Plasmids and genes contributing to high-level quinolone resistance in Escherichia coli. Int. J. Antimicrob. Agents 56, 105987 (2020).

    Article  PubMed  Google Scholar 

  152. Porse, A., Schønning, K., Munck, C. & Sommer, M. O. A. Survival and evolution of a large multidrug resistance plasmid in new clinical bacterial hosts. Mol. Biol. Evol. 33, 2860–2873 (2016).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  153. Venturini, C., Beatson, S. A., Djordjevic, S. P. & Walker, M. J. Multiple antibiotic resistance gene recruitment onto the enterohemorrhagic Escherichia coli virulence plasmid. FASEB J. 24, 1160–1166 (2010).

    Article  CAS  PubMed  Google Scholar 

  154. Harmer, C. J. & Hall, R. M. IS26 cannot move alone. J. Antimicrob. Chemother. 76, 1428–1432 (2021).

    Article  CAS  PubMed  Google Scholar 

  155. Dawes, F. E. et al. Distribution of class 1 integrons with IS26-mediated deletions in their 3′-conserved segments in Escherichia coli of human and animal origin. PLoS ONE 5, e12754 (2010).

    Article  PubMed Central  PubMed  Google Scholar 

  156. Harmer, C. J. & Hall, R. M. An analysis of the IS6/IS26 family of insertion sequences: is it a single family? Microb. Genom. 5, e000291 (2019).

    PubMed Central  PubMed  Google Scholar 

  157. Tedijanto, C., Olesen, S. W., Grad, Y. H. & Lipsitch, M. Estimating the proportion of bystander selection for antibiotic resistance among potentially pathogenic bacterial flora. Proc. Natl Acad. Sci. USA 115, E11988–E11995 (2018).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  158. Cummins, M. L. et al. Whole-genome sequence analysis of an extensively drug-resistant Salmonella enterica serovar Agona isolate from an Australian silver gull (Chroicocephalus novaehollandiae) reveals the acquisition of multidrug resistance plasmids. mSphere 5, e00743-20 (2020).

    Article  PubMed Central  PubMed  Google Scholar 

  159. Nyirabahizi, E. et al. Evaluation of Escherichia coli as an indicator for antimicrobial resistance in Salmonella recovered from the same food or animal ceca samples. Food Control. 115, 107280 (2020).

    Article  CAS  Google Scholar 

  160. United Nations Environment Programme. Environmental dimensions of antimicrobial resistance: summary for policymakers. https://wedocs.unep.org/bitstream/handle/20.500.11822/38373/antimicrobial_R.pdf (2022).

  161. Kohanski, M. A., Dwyer, D. J., Hayete, B., Lawrence, C. A. & Collins, J. J. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130, 797–810 (2007).

    Article  CAS  PubMed  Google Scholar 

  162. Miller, C. et al. SOS response induction by β-lactams and bacterial defense against antibiotic lethality. Science 305, 1629–1631 (2004).

    Article  CAS  PubMed  Google Scholar 

  163. Shapiro, R. S. Antimicrobial-induced DNA damage and genomic instability in microbial pathogens. PLoS Pathog. 11, e1004678 (2015).

    Article  PubMed Central  PubMed  Google Scholar 

  164. Cheng, Y.-Y. et al. Efficient plasmid transfer via natural competence in a microbial co-culture. Mol. Syst. Biol. 19, e11406 (2023).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  165. Fornelos, N., Browning, D. F. & Butala, M. The use and abuse of LexA by mobile genetic elements. Trends Microbiol. 24, 391–401 (2016).

    Article  CAS  PubMed  Google Scholar 

  166. Baharoglu, Z., Bikard, D. & Mazel, D. Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLoS Genet. 6, e1001165 (2010).

    Article  PubMed Central  PubMed  Google Scholar 

  167. Ginn, O. et al. Open waste canals as potential sources of antimicrobial resistance genes in aerosols in urban Kanpur, India. Am. J. Trop. Med. Hyg. 104, 1761–1767 (2021).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  168. Karkman, A., Pärnänen, K. & Larsson, D. G. J. Fecal pollution can explain antibiotic resistance gene abundances in anthropogenically impacted environments. Nat. Commun. 10, 80 (2019).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  169. Dolejska, M. & Papagiannitsis, C. C. Plasmid-mediated resistance is going wild. Plasmid 99, 99–111 (2018).

    Article  CAS  PubMed  Google Scholar 

  170. Snaith, A. E. et al. The highly diverse plasmid population found in Escherichia coli colonizing travellers to Laos and its role in antimicrobial resistance gene carriage. Microb. Genom. 9, 001000 (2023).

    CAS  Google Scholar 

  171. Rodríguez-Molina, D. et al. International travel as a risk factor for carriage of extended-spectrum β-lactamase-producing Escherichia coli in a large sample of European individuals—The AWARE Study. Int. J. Environ. Res. Public Health 19, 4758 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  172. Ginn, O. et al. Detection and quantification of enteric pathogens in aerosols near open wastewater canals in cities with poor sanitation. Environ. Sci. Technol. 55, 14758–14771 (2021). This study emphasizes that aerosols generated in densely populated regions with comparatively poor sanitation practices are under-recognized as a mechanism of transmission of ARGs and enteric pathogens.

    Article  CAS  PubMed  Google Scholar 

  173. Xin, H. et al. Animal farms are hot spots for airborne antimicrobial resistance. Sci. Total Environ. 851, 158050 (2022).

    Article  CAS  PubMed  Google Scholar 

  174. Lv, B. et al. Abundances and profiles of antibiotic resistance genes as well as co-occurrences with human bacterial pathogens in ship ballast tank sediments from a shipyard in Jiangsu Province, China. Ecotoxicol. Environ. Saf. 157, 169–175 (2018).

    Article  CAS  PubMed  Google Scholar 

  175. Lv, B. et al. Vessel transport of antibiotic resistance genes across oceans and its implications for ballast water management. Chemosphere 253, 126697 (2020).

    Article  CAS  PubMed  Google Scholar 

  176. Elankumaran, P., Browning, G. F., Marenda, M. S., Reid, C. J. & Djordjevic, S. P. Close genetic linkage between human and companion animal extraintestinal pathogenic Escherichia coli ST127. Curr. Res. Microb. Sci. 3, 100106 (2022).

    CAS  PubMed Central  PubMed  Google Scholar 

  177. Abdullahi, I. N. et al. Clonal relatedness of coagulase-positive staphylococci among healthy dogs and dog-owners in Spain. Detection of multidrug-resistant-MSSA-CC398 and novel linezolid-resistant-MRSA-CC5. Front. Microbiol. 14, 1121564 (2023).

    Article  PubMed Central  PubMed  Google Scholar 

  178. Yang, Q. E. et al. Environmental dissemination of mcr-1 positive Enterobacteriaceae by Chrysomya spp. (common blowfly): an increasing public health risk. Environ. Int. 122, 281–290 (2019). This study sheds light on the role of blow flies in disseminating clinically important ARGs, particularly in resource-poor environments.

    Article  CAS  PubMed  Google Scholar 

  179. Tyrrell, C. et al. Differential impact of swine, bovine and poultry manure on the microbiome and resistome of agricultural grassland. Sci. Total Environ. 886, 163926 (2023).

    Article  CAS  PubMed  Google Scholar 

  180. Marutescu, L. G. et al. Insights into the impact of manure on the environmental antibiotic residues and resistance pool. Front. Microbiol. 13, 965132 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

  181. Klein, E. Y. et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc. Natl Acad. Sci. USA 115, E3463–E3470 (2018).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  182. Kuppusamy, S. et al. Veterinary antibiotics (VAs) contamination as a global agro-ecological issue: a critical view. Agric. Ecosyst. Environ. 257, 47–59 (2018).

    Article  CAS  Google Scholar 

  183. Ma, F., Xu, S., Tang, Z., Li, Z. & Zhang, L. Use of antimicrobials in food animals and impact of transmission of antimicrobial resistance on humans. Biosaf. Health 3, 32–38 (2021).

    Article  Google Scholar 

  184. Tiseo, K., Huber, L., Gilbert, M., Robinson, T. P. & Van Boeckel, T. P. Global trends in antimicrobial use in food animals from 2017 to 2030. Antibiotics 9, E918 (2020).

    Article  Google Scholar 

  185. Van Boeckel, T. P. et al. Global trends in antimicrobial use in food animals. Proc. Natl Acad. Sci. USA 112, 5649–5654 (2015).

    Article  PubMed Central  PubMed  Google Scholar 

  186. Kemper, N. Veterinary antibiotics in the aquatic and terrestrial environment. Ecol. Indic. 8, 1–13 (2008).

    Article  CAS  Google Scholar 

  187. Zhang, N. et al. Coexistence between antibiotic resistance genes and metal resistance genes in manure-fertilized soils. Geoderma 382, 114760 (2021).

    Article  CAS  Google Scholar 

  188. Berendes, D. M., Yang, P. J., Lai, A., Hu, D. & Brown, J. Estimation of global recoverable human and animal faecal biomass. Nat. Sustain. 1, 679–685 (2018). This study estimates the global production of human and animal faeces, emphasizing the increasing animal to human ratio with time (6:1 by 2050), and highlights the importance of managing the persistent threats to global public health particularly in LMICs as well as the opportunities for recovery of resources via circular economies, with implications for zoonosis, One Health and AMR.

    Article  Google Scholar 

  189. Cavicchioli, R. et al. Scientists’ warning to humanity: microorganisms and climate change. Nat. Rev. Microbiol. 17, 569–586 (2019).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  190. MacFadden, D. R., McGough, S. F., Fisman, D., Santillana, M. & Brownstein, J. S. Antibiotic resistance increases with local temperature. Nat. Clim. Change 8, 510–514 (2018).

    Article  CAS  Google Scholar 

  191. McGough, S. F., MacFadden, D. R., Hattab, M. W., Mølbak, K. & Santillana, M. Rates of increase of antibiotic resistance and ambient temperature in Europe: a cross-national analysis of 28 countries between 2000 and 2016. Eurosurveillance 25, 1900414 (2020).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  192. Walsh, T. R., Weeks, J., Livermore, D. M. & Toleman, M. A. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect. Dis. 11, 355–362 (2011).

    Article  PubMed  Google Scholar 

  193. Reckien, D. & Aalst, M. K. van. in Climate Change 2022: Impacts, Adaptation and Vulnerability: Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Pörtner, H.O, Roberts, D.C, Tignor, M., Poloczanska, E.S., Mintenbeck, K., Alegría, A., Craig, M., Langsdorf, S., Löschke, S., Möller, V., Okem, A., Rama, B. (eds.), 3–33 (Cambridge Univ. Press, 2022).

  194. Fouladkhah, A. C., Thompson, B. & Camp, J. S. The threat of antibiotic resistance in changing climate. Microorganisms 8, E748 (2020).

    Article  Google Scholar 

  195. Delgado-Baquerizo, M. et al. The proportion of soil-borne pathogens increases with warming at the global scale. Nat. Clim. Chang. 10, 550–554 (2020).

    Article  Google Scholar 

  196. Escobar, L. E. et al. A global map of suitability for coastal Vibrio cholerae under current and future climate conditions. Acta Trop. 149, 202–211 (2015).

    Article  PubMed  Google Scholar 

  197. Mora, C. et al. Over half of known human pathogenic diseases can be aggravated by climate change. Nat. Clim. Chang. 12, 869–875 (2022).

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank F. MacIver from the University of Technology Sydney for assistance with preparing and editing the manuscript and S. Zufan from the University of Melbourne for assistance with preparation of Fig. 3. This work was supported by the Medical Research Future Fund (MRFF)-supported AusPathoGen Program (FSPGN000049) and by the Australian Centre for Genomic Epidemiological Microbiology (Ausgem), a collaborative research initiative between the New South Wales Department of Primary Industries and the University of Technology Sydney. B.P.H. is supported by a National Health and Medical Research Council (NHMRC) Fellowship (GNT1196103).

Author information

Authors and Affiliations

Authors

Contributions

S.P.D., V.M.J., T.S., M.L.C., A.E.W., B.D., E.D. and B.P.H. researched the literature. S.P.D., V.M.J., T.S., M.L.C., A.E.W., E.R.W., C.J.R., E.D. and B.P.H. contributed substantially to discussions of the content. S.P.D., V.M.J., T.S., M.L.C., E.D. and B.P.H. wrote the article. S.P.D., V.M.J., T.S., A.E.W., B.D., C.J.R., E.D. and B.P.H. reviewed and/or edited the manuscript before submission.

Corresponding author

Correspondence to Steven P. Djordjevic.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Reviews Genetics thanks Erick Denamur and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

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

Related links

hAMRonization: https://github.com/pha4ge/hAMRonization

PHA4GE Consortium: https://pha4ge.org/

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Djordjevic, S.P., Jarocki, V.M., Seemann, T. et al. Genomic surveillance for antimicrobial resistance — a One Health perspective. Nat Rev Genet 25, 142–157 (2024). https://doi.org/10.1038/s41576-023-00649-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41576-023-00649-y

Search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research