Terrestrial landscape impacts the biogeographic pattern of soil Escherichia coli via altering the strength of environmental selection and dispersal

Abstract

High-quality habitats for wildlife (e.g., forest) provide essential ecosystem services while increasing species diversity and habitat connectivity. Unfortunately, presence of such habitats adjacent to produce fields may increase risk for contamination of fruits and vegetables by enteric bacteria, including Escherichia coli. E. coli survives in extra-host environments (e.g., soil) and could disperse across landscapes by wildlife. Understanding how terrestrial landscapes impact the distribution of soil E. coli is of importance in assessing the contamination risk of agricultural products. Here, using multi-locus sequence typing, we characterized 938 E. coli soil isolates collected from two watersheds with different landscape patterns in New York state, USA, and compared the distribution of E. coli and the influence of two ecological forces (environmental selection and dispersal) on the distribution between these two watersheds. Results showed that for the watershed with widespread produce fields, sparse forests, and limited interaction between the two land-use types, E. coli composition was significantly different between produce field sites and forest sites; this distribution was shaped by relatively strong environmental selection likely from soil phosphorus and slight dispersal limitation. For the watershed with more forested areas and stronger interaction between produce field sites and forest sites, E. coli composition between these two land-use types was relatively homogeneous; this distribution appeared to a consequence of wildlife-driven dispersal, inferred by competing models. Collectively, our results suggest that terrestrial landscape attributes could impact the biogeographic pattern of enteric bacteria by adjusting the importance of environmental selection and dispersal. IMPORTANCEUnderstanding the ecology of enteric bacteria in extra-host environments is important to allow for development and implementation of strategies to minimize pre-harvest contamination of produce with enteric pathogens. Our findings suggest that watershed landscape is an important factor influencing the importance of ecological drivers and dispersal patterns of E. coli. For watersheds with widespread produce fields, E. coli appears to experience local adaptation, possibly due to exposure to environmental stresses associated with agricultural activities. In contrast, for watersheds with high forest coverage we found evidence for wildlife-driven dispersal of E. coli, which might facilitate more frequent genetic exchange in this environment. Agricultural areas in such watersheds may have a higher risk of produce contamination due to less environmental constraints and higher potential of dispersal of enteric bacteria between locations. The significance of our research lies in exploring ecological principles underlying the biogeographic pattern of enteric bacteria at the regional level, which can inform agricultural, environmental and public health scientists that aim to reduce the risk of food contamination by enteric bacteria.