Genomic surveillance for antimicrobial resistance - a One Health perspective

doi:10.1038/s41576-023-00649-y

Review

. 2024 Feb;25(2):142-157.

doi: 10.1038/s41576-023-00649-y. Epub 2023 Sep 25.

Genomic surveillance for antimicrobial resistance - a One Health perspective

Steven P Djordjevic^{1

2}, Veronica M Jarocki^{3

4}, Torsten Seemann^{5

6}, Max L Cummins^{3

4}, Anne E Watt⁶, Barbara Drigo^{7

8}, Ethan R Wyrsch^{3

4}, Cameron J Reid^{3

4}, Erica Donner^{8

9}, Benjamin P Howden^{5

6}

Affiliations

¹ Australian Institute for Microbiology and Infection, University of Technology Sydney, Sydney, New South Wales, Australia. steven.djordjevic@uts.edu.au.
² Australian Centre for Genomic Epidemiological Microbiology, University of Technology Sydney, Sydney, New South Wales, Australia. steven.djordjevic@uts.edu.au.
³ Australian Institute for Microbiology and Infection, University of Technology Sydney, Sydney, New South Wales, Australia.
⁴ Australian Centre for Genomic Epidemiological Microbiology, University of Technology Sydney, Sydney, New South Wales, Australia.
⁵ Centre for Pathogen Genomics, University of Melbourne, Melbourne, Victoria, Australia.
⁶ Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, University of Melbourne at the Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia.
⁷ UniSA STEM, University of South Australia, Adelaide, South Australia, Australia.
⁸ Future Industries Institute, University of South Australia, Adelaide, South Australia, Australia.
⁹ Cooperative Research Centre for Solving Antimicrobial Resistance in Agribusiness, Food, and Environments (CRC SAAFE), Adelaide, South Australia, Australia.

PMID: 37749210
DOI: 10.1038/s41576-023-00649-y

Review

Genomic surveillance for antimicrobial resistance - a One Health perspective

Steven P Djordjevic et al. Nat Rev Genet. 2024 Feb.

. 2024 Feb;25(2):142-157.

doi: 10.1038/s41576-023-00649-y. Epub 2023 Sep 25.

Authors

Affiliations

¹ Australian Institute for Microbiology and Infection, University of Technology Sydney, Sydney, New South Wales, Australia. steven.djordjevic@uts.edu.au.
² Australian Centre for Genomic Epidemiological Microbiology, University of Technology Sydney, Sydney, New South Wales, Australia. steven.djordjevic@uts.edu.au.
³ Australian Institute for Microbiology and Infection, University of Technology Sydney, Sydney, New South Wales, Australia.
⁴ Australian Centre for Genomic Epidemiological Microbiology, University of Technology Sydney, Sydney, New South Wales, Australia.
⁵ Centre for Pathogen Genomics, University of Melbourne, Melbourne, Victoria, Australia.
⁶ Microbiological Diagnostic Unit Public Health Laboratory, Department of Microbiology and Immunology, University of Melbourne at the Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia.
⁷ UniSA STEM, University of South Australia, Adelaide, South Australia, Australia.
⁸ Future Industries Institute, University of South Australia, Adelaide, South Australia, Australia.
⁹ Cooperative Research Centre for Solving Antimicrobial Resistance in Agribusiness, Food, and Environments (CRC SAAFE), Adelaide, South Australia, Australia.

PMID: 37749210
DOI: 10.1038/s41576-023-00649-y

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.

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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. - PMC - DOI - PubMed
1. 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. - DOI
1. Gillings, M. R. Lateral gene transfer, bacterial genome evolution, and the Anthropocene. Ann. N. Y. Acad. Sci. 1389, 20–36 (2017). - DOI - PubMed
1. Christaki, E., Marcou, M. & Tofarides, A. Antimicrobial resistance in bacteria: mechanisms, evolution, and persistence. J. Mol. Evol. 88, 26–40 (2020). - DOI - PubMed
1. 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). - DOI - PubMed

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[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. - PMC - DOI - PubMed

[2] 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. - PMC - DOI - PubMed

[3] 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. - DOI

[4] 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. - DOI

[5] Gillings, M. R. Lateral gene transfer, bacterial genome evolution, and the Anthropocene. Ann. N. Y. Acad. Sci. 1389, 20–36 (2017). - DOI - PubMed

[6] Gillings, M. R. Lateral gene transfer, bacterial genome evolution, and the Anthropocene. Ann. N. Y. Acad. Sci. 1389, 20–36 (2017). - DOI - PubMed

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

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

[9] 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). - DOI - PubMed

[10] 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). - DOI - PubMed

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Genomic surveillance for antimicrobial resistance - a One Health perspective

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Genomic surveillance for antimicrobial resistance - a One Health perspective

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