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, we compared the distribution of E. coli isolated from soils from two watersheds with different landscape patterns in central New York, USA, and examined the influences of two ecological forces - environmental selection and dispersal - on the distribution of E. coli. Results showed that for the watershed with widespread produce fields, sparse forests, and limited interaction between the two land types, E. coli composition was significantly different between produce field and forest; this distribution was shaped by relatively strong environmental selection likely triggered by soil phosphorus and antimony. For the watershed with more forested areas and stronger interaction between produce field and forest, E. coli composition between these two land types was relatively homogeneous; this distribution was a consequence of weak selective pressure potentially from soil moisture and wildlife-driven dispersal by small flocking insectivore/granivores and large nuisance wildlife, which were identified as potential vehicles by competing models. Collectively, our results suggest that terrestrial landscape could drive the biogeographic pattern of enteric bacteria by adjusting the balance between environmental selection and dispersal. IMPORTANCE Understanding the ecology of enteric bacteria in extra-host environments is important to allow for development and implementation of strategies to minimize pre-harvest contamination with enteric pathogens. Our findings suggest that watershed landscape is an important factor influencing the ecological drivers and transmission pattern of E. coli. For watersheds with widespread produce fields, E. coli appears to experience local adaptation, likely due to exposure to environmental stresses possibly 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 constrains and higher potential of transmission 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 policies that aim to reduce the risk of food contamination by enteric bacteria.