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Foodborne bacterial pathogens: genome-based approaches for enduring and emerging threats in a complex and changing world

Nature Reviews Microbiology volume 22, pages 543–555 (2024)Cite this article

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Abstract

Foodborne illnesses pose a substantial health and economic burden, presenting challenges in prevention due to the diverse microbial hazards that can enter and spread within food systems. Various factors, including natural, political and commercial drivers, influence food production and distribution. The risks of foodborne illness will continue to evolve in step with these drivers and with changes to food systems. For example, climate impacts on water availability for agriculture, changes in food sustainability targets and evolving customer preferences can all have an impact on the ecology of foodborne pathogens and the agrifood niches that can carry microorganisms. Whole-genome and metagenome sequencing, combined with microbial surveillance schemes and insights from the food system, can provide authorities and businesses with transformative information to address risks and implement new food safety interventions across the food chain. In this Review, we describe how genome-based approaches have advanced our understanding of the evolution and spread of enduring bacterial foodborne hazards as well as their role in identifying emerging foodborne hazards. Furthermore, foodborne hazards exist in complex microbial communities across the entire food chain, and consideration of these co-existing organisms is essential to understanding the entire ecology supporting pathogen persistence and transmission in an evolving food system.

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Fig. 1: Ecological and socioeconomic drivers that may shape the microbial landscape of food and food production systems.
Fig. 2: Relationship between pathogen populations and the dynamics of foodborne illness.
Fig. 3: International impacts and prioritization of bacterial foodborne illness.
Fig. 4: One Health approach to ecological frameworks and epidemiology in food safety.
Fig. 5: Tracing bacterial hazards in the food chain.
Fig. 6: The impact of high-resolution WGS on the detection and resolution of foodborne outbreaks.

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Acknowledgements

A.E.M. and M.W.G. are supported by the Biotechnology and Biological Sciences Research Council (BBSRC) Institute Strategic Programme Microbes and Food Safety BB/X011011/1 and its constituent project BBS/E/F/000PR13634 (Theme 1, Microbial threats from foods in established and evolving food systems). This work was also supported in part by BBSRC grants BB/V018221/1 and BB/X002985/1 (UK Food Safety Research Network). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Authors and Affiliations

  1. Quadram Institute Bioscience, Norwich, UK

    Alison E. Mather & Matthew W. Gilmour

  2. University of East Anglia, Norwich, UK

    Alison E. Mather & Matthew W. Gilmour

  3. Royal Veterinary College, Hatfield, UK

    Stuart W. J. Reid

  4. Tāuwharau Ora, School of Veterinary Science, Te Kunenga Ki Pūrehuroa, Massey University, Papaioea, Palmerston North, Aotearoa New Zealand

    Nigel P. French

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The authors contributed equally to all aspects of the article.

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Correspondence to Alison E. Mather.

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Competing interests

International Patent Application No. PCT/GB2023/050906 entitled “Determination and quantification of the microbial communities and antimicrobial resistance genes on food” in the name of Quadram Institute Bioscience has been filed (priority date 05/04/2022) and is currently in the international phase; A.E.M. is an inventor. This relates to the aspect of the Review where it is mentioned that the potential detection of pathogens through metagenomics can be affected by the amount of contaminating host DNA and sequencing depth. N.P.F. is a member of the International Commission on Microbiological Specifications for Foods (ICMSF) and an Emeritus Director of the New Zealand Food Safety Science and Research Centre. Both organizations receive support from the food industry and government agencies. Both roles are unpaid and advisory, and related to food safety research, and neither organization influenced the content contributed by N.P.F. to the Review. The other authors declare no competing interests.

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Nature Reviews Microbiology thanks Steven Djordjevic, who co-reviewed with Veronica Jarocki; Jasna Kovac; and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Mather, A.E., Gilmour, M.W., Reid, S.W.J. et al. Foodborne bacterial pathogens: genome-based approaches for enduring and emerging threats in a complex and changing world. Nat Rev Microbiol 22, 543–555 (2024). https://doi.org/10.1038/s41579-024-01051-z

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