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Soil salinity, pH, and indigenous bacterial community interactively influence the survival of E. coli O157:H7 revealed by multivariate statistics

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Abstract

Complexities of biotic-abiotic interactions in soils result in the lack of integrated understanding of environmental variables that restrict the survival of shiga toxin-producing E. coli O157:H7. Herein, we reanalyzed previously published data and highlighted the influence of soil abiotic factors on E. coli O157:H7 survivability and elucidated how these factors took effect indirectly through affecting indigenous bacterial community. Interaction network analysis indicated salinity and pH decreased the relative abundances of some bacterial taxa (e.g., Acidobacteria_Gp4, Acidobacteria_Gp6, and Deltaproteobacteria) which were positively correlated with the survival of E. coli O157:H7 in soils, and vice versa (e.g., Gammaproteobacteria and Flavobacteria) (P < 0.05). An array of multivariate statistical approaches including partial Mantel test, variation partition analysis (VPA), and structural equation model (SEM) further confirmed that biotic and abiotic factors interactively shaped the survival profile of E. coli O157:H7. This study revealed that some bacterial taxa were correlated with survival of E. coli O157:H7 directly, and salinity and pH could affect E. coli O157:H7 survival through changing these bacterial taxa. These findings suggest that salinity in soil might benefit the control of fecal pathogenic E. coli invasion, while soil acidification caused by anthropogenic influences could potentially increase the persistence of E. coli O157:H7 in agro-ecosystem.

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Data availability

The sequencing data could be downloaded in https://www.ars.usda.gov/ARSUSERFILES/20361500/PUBLIC%20DATA/SALINITY%20PRODUCE%20SEQUENCING%20DATA%202010-2015.ZIP.

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Acknowledgments

We thank Drs. Jorge Fonseca of the University of Arizona Yuma, Mark Trent, UC-Davis, Imperial Agricultural Experiment Station, and James McCreight of USDA-ARS Salinas, CA for providing soil samples for this study. We also thank Damon Baptista for technical help and Qiuting Zhang for statistical analysis.

Funding

This research was financed by the National Natural Science Foundation of China (no. 41571304), CSREES NIFA Agreement 2008-35201-18709, and the 206 Manure and Byproduct Utilization Project of the USDA-ARS.

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Authors and Affiliations

  1. Key Laboratory of Ground Water Resource and Environment, Ministry of Education, Jilin University, Changchun, 130021, China

    Ziming Han & Jincai Ma

  2. Jilin Provincial Key Laboratory of Water Resources and Environment, Jilin University, Changchun, 130021, China

    Ziming Han & Jincai Ma

  3. State Key Laboratory of Environmental Aquatic Chemistry, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China

    Ziming Han

  4. College of New Energy and Environment, Jilin University, Changchun, 130021, China

    Jincai Ma

  5. Department of Biological Sciences, University of Wisconsin, Milwaukee, WI, USA

    Ching-Hong Yang

  6. USDA-ARS U. S. Salinity Laboratory, Riverside, CA, USA

    Abasiofiok Mark Ibekwe

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  1. Ziming Han
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  2. Jincai Ma
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  4. Abasiofiok Mark Ibekwe
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Contributions

Ziming Han: conceptualization, methodology, formal analysis, and writing—original draft preparation; Jincai Ma: methodology, conceptualization, supervision, funding acquisition, and writing—reviewing and editing; Abasiofiok Mark Ibekwe: project administration, funding acquisition, resources, and writing—reviewing and editing; Ching-Hong Yang: methodology and writing—reviewing and editing. All authors read and approved the final manuscript.

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Correspondence to Jincai Ma.

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ESM 1

Additional experimental methodology showed survival experiment of E. coli O157:H7 in soils and survival data modeling; additional tables related to correlation analysis among survival parameters, physicochemical properties, and bacterial groups; additional figures were comparisons of survival parameters, salinity, pH, and bacterial community among different sampling sites, concentrations of Na+, K+, Ca2+, and Mg2+ in soil water extracts, and the relationships between soil physicochemical properties and accumulated bacterial class abundance. (DOCX 3.86 MB)

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Han, Z., Ma, J., Yang, CH. et al. Soil salinity, pH, and indigenous bacterial community interactively influence the survival of E. coli O157:H7 revealed by multivariate statistics. Environ Sci Pollut Res 28, 5575–5586 (2021). https://doi.org/10.1007/s11356-020-10942-6

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