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Available phosphorus and opportunistic pathogens drive geographic variation in Escherichia coli O157:H7 survival in soils across eastern China

Abstract

The persistence of food-borne pathogens in soil can trigger disease outbreaks, highlighting the critical need to understand their survival patterns. Here we investigate the survival of Escherichia coli O157:H7, a notable food-borne pathogen, across 81 natural soils from eastern China using inoculation experiments. E. coli O157:H7 survival ranged from 2.0 days to 43.3 days in soils. The survival-time map revealed hotspots and geographical heterogeneity of E. coli O157:H7 survival across eastern China. Bioinformatics analysis and validation experiments identified available phosphorus as the major factor controlling E. coli O157:H7 survival, with higher available phosphorus content in soils extending their survival. Two opportunistic pathogens, Enterococcus faecium and Aerococcus viridans, facilitated E. coli O157:H7 survival by forming biofilm structures and cross-feeding, respectively. Climate factors showed mostly indirect correlations with E. coli O157:H7. These findings enhance our understanding of food-borne pathogen survival in soils and offer insights to inform agricultural practices for preventing and controlling outbreaks.

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Fig. 1: Geographic heterogeneity of E. coli O157:H7 survival in eastern China (n = 81).
Fig. 2: Correlations of climate factors and soil physicochemical properties with E. coli O157:H7 survival time in soils (n = 39).
Fig. 3: Relationships between bacterial diversity, bacterial network, functional genes and E. coli O157:H7 survival time (n = 39).
Fig. 4: Validation experiments to assess abiotic and biotic factors and promotional mechanisms.
Fig. 5: Relationships between E. coli O157:H7 survival and biotic and abiotic factors.

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Data availability

The sequence data that support the findings of this study are available in the NCBI database as PRJNA1030546. Source data are provided with this paper.

Code availability

No custom code was developed for use in this paper. Code used for statistical analyses in this study is available via GitHub at https://github.com/zhangnan1997/Geographic-heterogeneity-and-drivers-of Escherichia-coli-O157-H7-survival-in-soils.

References

  1. Baker, R. E. et al. Infectious disease in an era of global change. Nat. Rev. Microbiol. 20, 193–205 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Li, M. et al. Natural host–environmental media–human: a new potential pathway of COVID-19 outbreak. Engineering 6, 1085–1098 (2020).

    Article  CAS  PubMed  Google Scholar 

  3. Levy, J. I., Andersen, K. G., Knight, R. & Karthikeyan, S. Wastewater surveillance for public health. Science 379, 26–27 (2023).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  4. Raymenants, J. et al. Indoor air surveillance and factors associated with respiratory pathogen detection in community settings in Belgium. Nat. Commun. 14, 1332 (2023).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  5. Zhu, D., Zhang, Y. & Zhu, Y. Human pathogens in the soil ecosystem: occurrence, dispersal, and study method. Curr. Opin. Environ. Sci. Health 33, 100471 (2023).

    Article  Google Scholar 

  6. Samaddar, S. et al. Role of soil in the regulation of human and plant pathogens: soils’ contributions to people. Philos. Trans. R. Soc. B 376, 20200179 (2021).

    Article  Google Scholar 

  7. Todd-Searle, J. et al. Quantification of Salmonella enterica transfer between tomatoes, soil, and plastic mulch. Int. J. Food Microbiol. 316, 108480 (2020).

    Article  CAS  PubMed  Google Scholar 

  8. Alegbeleye, O. & Sant’Ana, A. S. Survival of Salmonella spp. under varying temperature and soil conditions. Sci. Total Environ. 884, 163744 (2023).

    Article  CAS  PubMed  Google Scholar 

  9. van Elsas, J. D., Semenov, A. V., Costa, R. & Trevors, J. T. Survival of Escherichia coli in the environment: fundamental and public health aspects. ISME J. 5, 173–183 (2011).

    Article  PubMed  Google Scholar 

  10. Liu, B. et al. Enterohaemorrhagic E. coli utilizes host- and microbiota-derived l-malate as a signaling molecule for intestinal colonization. Nat. Commun. 14, 7227 (2023).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  11. Rangel, J. M., Sparling, P. H., Crowe, C., Griffin, P. M. & Swerdlow, D. L. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982–2002. Emerg. Infect. Dis. 11, 603–609 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Anderson, J. D. et al. Burden of enterotoxigenic Escherichia coli and shigella non-fatal diarrhoeal infections in 79 low-income and lower middle-income countries: a modelling analysis. Lancet. Glob. Health 7, e321–e330 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Khalil, I. A. et al. Morbidity and mortality due to shigella and enterotoxigenic Escherichia coli diarrhoea: the Global Burden of Disease Study 1990–2016. Lancet Infect. Dis. 18, 1229–1240 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Interagency Food Safety Analytics Collaboration. Foodborne Illness Source Attribution Estimates for Salmonella, Escherichia coli O157, and Listeria monocytogenes—United States 2021 Annual Report (Centers for Disease Control and Prevention, 2023).

  15. Rodwell, E. V., Greig, D. R., Godbole, G. & Jenkins, C. Clinical and public health implications of increasing notifications of LEE-negative Shiga toxin-producing Escherichia coli in England, 2014–2022. J. Med. Microbiol. 73, 001790 (2024).

    Article  CAS  Google Scholar 

  16. Jones, G. et al. Sporadic Shiga toxin-producing Escherichia coli-associated pediatric hemolytic uremic syndrome, France, 2012–2021. Emerg. Infect. Dis. 29, 2054 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Bai, X. et al. Prevalence and characteristics of Shiga toxin-producing Escherichia coli isolated from retail raw meats in China. Int. J. Food Microbiol. 200, 31–38 (2015).

    Article  CAS  PubMed  Google Scholar 

  18. 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 

  19. Mohanapriya, R., Paranidharan, V., Karthikeyan, S. & Balachandar, D. Surveillance and source tracking of foodborne pathogens in the vegetable production systems of India. Food Control 162, 110427 (2024).

    Article  Google Scholar 

  20. Işık, S., Çetin, B. & Topalcengiz, Z. Transfer of Salmonella, Escherichia coli O157:H7 and Listeria monocytogenes from contaminated soilless substrate and seeds to microgreens. Int. J. Food Microbiol. 414, 110612 (2024).

    Article  PubMed  Google Scholar 

  21. Wang, H. et al. A glimpse of Escherichia coli O157:H7 survival in soils from eastern China. Sci. Total Environ. 476-477, 49–56 (2014).

    Article  ADS  CAS  PubMed  Google Scholar 

  22. Han, Z. et al. Disentangling survival of Escherichia coli O157:H7 in soils: from a subpopulation perspective. Sci. Total Environ. 749, 141649 (2020).

    Article  CAS  PubMed  Google Scholar 

  23. Meyers, B. C. & McLellan, S. L. Influence of nutrients and the native community on E. coli survival in the beach environment. Appl. Environ. Microbiol. 88, e0104322 (2022).

    Article  PubMed  Google Scholar 

  24. Zhang, N. et al. Indigenous microbial community governs the survival of Escherichia coli O157:H7 in constructed wetlands. J. Environ. Manage. 334, 117524 (2023).

    Article  CAS  PubMed  Google Scholar 

  25. Liang, C. et al. Sediment pH, not the bacterial diversity, determines Escherichia coli O157:H7 survival in estuarine sediments. Environ. Pollut. 252, 1078–1086 (2019).

    Article  CAS  PubMed  Google Scholar 

  26. Xing, J., Wang, H., Brookes, P. C., Salles, J. F. & Xu, J. Soil pH and microbial diversity constrain the survival of E. coli in soil. Soil Biol. Biochem. 128, 139–149 (2019).

    Article  CAS  Google Scholar 

  27. van Elsas, J. D. et al. Survival of genetically marked Escherichia coli O157:H7 in soil as affected by soil microbial community shifts. ISME J. 1, 204–214 (2007).

    Article  PubMed  Google Scholar 

  28. Wang, H. Z. et al. Response of Escherichia coli O157:H7 survival to pH of cultivated soils. J. Soils Sediments 14, 1841–1849 (2014).

    Article  CAS  Google Scholar 

  29. Yao, Z. et al. Survival of Escherichia coli O157:H7 in soils from vegetable fields with different cultivation patterns. Appl. Environ. Microbiol. 79, 1755–1756 (2013).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  30. Yao, Z., Yang, L., Wang, H., Wu, J. & Xu, J. Fate of Escherichia coli O157: H7 in agricultural soils amended with different organic fertilizers. J. Hazard. Mater. 296, 30–36 (2015).

    Article  CAS  PubMed  Google Scholar 

  31. Zhang, T., Hu, S. & Yang, W. Variations of Escherichia coli O157:H7 survival in purple soils. Int. J. Environ. Res. Public Health 14, 1246 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Xiong, Y. W. et al. A novel Escherichia coli O157:H7 clone causing a major hemolytic uremic syndrome outbreak in China. PLoS ONE 7, e36144 (2012).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  33. Yang, C. et al. Outbreak dynamics of foodborne pathogen Vibrio parahaemolyticus over a seventeen year period implies hidden reservoirs. Nat. Microbiol. 7, 1221–1229 (2022).

    Article  CAS  PubMed  Google Scholar 

  34. Palmer, J. S., Hough, R. L., West, H. M. & Avery, L. M. A review of the abundance, behaviour and detection of clostridial pathogens in agricultural soils. Eur. J. Soil Sci. 70, 911–929 (2019).

    Article  Google Scholar 

  35. 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).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  36. van Elsas, J. D. et al. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc. Natl Acad. Sci. USA 109, 1159–1164 (2012).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  37. Van Mooy, B. A. S. et al. Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458, 69–72 (2009).

    Article  ADS  PubMed  Google Scholar 

  38. Oliverio, A. M. et al. The role of phosphorus limitation in shaping soil bacterial communities and their metabolic capabilities. mBio 11, 01718–01720 (2020).

    Article  Google Scholar 

  39. Chen, J. et al. Microbial phosphorus recycling in soil by intra- and extracellular mechanisms. ISME Commun. 3, 135 (2024).

    Article  Google Scholar 

  40. Mallon, C. A. et al. The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader’s niche. ISME J. 12, 728–741 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Su, M. et al. Phosphorus deficiency in soils with red color: insights from the interactions between minerals and microorganisms. Geoderma. 404, 115311 (2021).

    Article  ADS  CAS  Google Scholar 

  42. Spohn, M. & Schleuss, P. Addition of inorganic phosphorus to soil leads to desorption of organic compounds and thus to increased soil respiration. Soil Biol. Biochem. 130, 220–226 (2019).

    Article  CAS  Google Scholar 

  43. Dal Bello, M., Lee, H., Goyal, A. & Gore, J. Resource–diversity relationships in bacterial communities reflect the network structure of microbial metabolism. Nat. Ecol. Evol. 5, 1424–1434 (2021).

    Article  PubMed  Google Scholar 

  44. Cossart, P. & Sansonetti, P. J. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304, 242–248 (2004).

    Article  ADS  CAS  PubMed  Google Scholar 

  45. Huus, K. E. et al. Cross-feeding between intestinal pathobionts promotes their overgrowth during undernutrition. Nat. Commun. 12, 6860 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  46. Semenec, L. et al. Cross-protection and cross-feeding between Klebsiella pneumoniae and Acinetobacter baumannii promotes their co-existence. Nat. Commun. 14, 702 (2023).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  47. Dong, J. et al. The coexistence of bacterial species restructures biofilm architecture and increases tolerance to antimicrobial agents. Microbiol. Spectr. 11, e0358122 (2023).

    Article  PubMed  Google Scholar 

  48. Chitlapilly Dass, S. et al. Impact of mixed biofilm formation with environmental microorganisms on E. coli O157:H7 survival against sanitization. npj Sci. Food 4, 16 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Zhou, X. et al. Cross-kingdom synthetic microbiota supports tomato suppression of Fusarium wilt disease. Nat. Commun. 13, 7890 (2022).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  50. Suleiman, A. K. A. et al. Temporal variability of soil microbial communities after application of dicyandiamide-treated swine slurry and mineral fertilizers. Soil Biol. Biochem. 97, 71–82 (2016).

    Article  CAS  Google Scholar 

  51. Jiao, S., Yang, Y., Xu, Y., Zhang, J. & Lu, Y. Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across eastern China. ISME J. 14, 202–216 (2020).

    Article  PubMed  Google Scholar 

  52. Ma, J., Ibekwe, A. M., Crowley, D. E. & Yang, C. Persistence of Escherichia coli O157:H7 in major leafy green producing soils. Environ. Sci. Technol. 46, 12154–12161 (2012).

    Article  ADS  CAS  PubMed  Google Scholar 

  53. Mafart, P., Couvert, O., Gaillard, S. & Leguerinel, I. On calculating sterility in thermal preservation methods: application of the Weibull frequency distribution model. Int. J. Food Microbiol. 72, 107–113 (2002).

    Article  CAS  PubMed  Google Scholar 

  54. Baumgart, M. et al. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn’s disease involving the ileum. ISME J. 1, 403–418 (2007).

    Article  CAS  PubMed  Google Scholar 

  55. McLellan, S. L. et al. Universal microbial indicators provide surveillance of sewage contamination in harbours worldwide. Nat. Water 2, 1061–1070 (2024).

    Article  Google Scholar 

  56. Kulkarni, O. S. et al. Volatile methyl jasmonate from roots triggers host-beneficial soil microbiome biofilms. Nat. Chem. Biol. 20, 473–483 (2024).

    Article  CAS  PubMed  Google Scholar 

  57. Yang, X. et al. Loss of microbial diversity weakens specific soil functions, but increases soil ecosystem stability. Soil Biol. Biochem. 177, 108916 (2023).

    Article  CAS  Google Scholar 

  58. Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Li, D., Liu, C., Luo, R., Sadakane, K. & Lam, T. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676 (2015).

    Article  CAS  PubMed  Google Scholar 

  60. Lu, J. et al. Metagenome analysis using the Kraken software suite. Nat. Protoc. 17, 2815–2839 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Bowers, R. M. et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat. Biotechnol. 35, 725–731 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Lu, J., Breitwieser, F. P., Thielen, P. & Salzberg, S. L. Bracken: estimating species abundance in metagenomics data. PeerJ Comput. Sci. 3, e104 (2017).

    Article  PubMed  Google Scholar 

  63. Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Qian, L. et al. MCycDB: a curated database for comprehensively profiling methane cycling processes of environmental microbiomes. Mol. Ecol. Resour. 22, 1803–1823 (2022).

    Article  CAS  PubMed  Google Scholar 

  66. Tu, Q., Lin, L., Cheng, L., Deng, Y. & He, Z. NCycDB: a curated integrative database for fast and accurate metagenomic profiling of nitrogen cycling genes. Bioinformatics 35, 1040–1048 (2019).

    Article  CAS  PubMed  Google Scholar 

  67. Zeng, J. et al. PCycDB: a comprehensive and accurate database for fast analysis of phosphorus cycling genes. Microbiome 10, 101 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Ge, Z. B. et al. Two-tiered mutualism improves survival and competitiveness of cross-feeding soil bacteria. ISME J. 17, 2090–2102 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are grateful for the financial support of the National Natural Science Foundation of China (grant numbers 41721001 to J. Xu, 423B2701 to N.Z. and 42090060 to B.M.). We thank X. Zhao, X. Zhang, X. Zheng and X. Yu of the Analysis Center of Agriculture, Life and Environment Sciences, Zhejiang University, for their technical assistance.

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J. Xu acquired funding and contributed to the experimental design, study supervision, soil collection, interpretation of the results, and writing, review and editing. N.Z. acquired funding and contributed to the writing, data analysis, figure visualization and validation experiments. Z.Y. contributed to the soil collection and physicochemical characterization. T.Z. contributed to the soil collection and physicochemical characterization. J. Xing contributed to the investigation and formal analysis. H.W. contributed to the review. Z.J. contributed to the investigation. R.A.D. contributed to the review and editing. B.M. acquired funding and contributed to the soil collection, data analysis and review.

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Correspondence to Jianming Xu.

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Xu, J., Zhang, N., Yao, Z. et al. Available phosphorus and opportunistic pathogens drive geographic variation in Escherichia coli O157:H7 survival in soils across eastern China. Nat Food 6, 777–786 (2025). https://doi.org/10.1038/s43016-025-01191-2

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