High ammonium levels and soil moisture are strong drivers of Escherichia coli survival and microbial community dynamics in compost-amended soils

Authors: CUTLER, ANYA - University Of Vermont; WEICHT, THOMAS - University Of Vermont; Sharma, Manan; Buyer, Jeffrey; Millner, Patricia; NEHER, DEBORAH - University Of Vermont

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/25/2019
Publication Date: 5/10/2019
Citation: Cutler, A., Weicht, T., Sharma, M., Buyer, J.S., Millner, P.D., Neher, D. 2019. High ammonium levels and soil moisture are strong drivers of Escherichia coli survival and microbial community dynamics in compost-amended soils. Applied and Environmental Microbiology. 126:1910-1922. https://doi.org/10.1111/jam.14268.
DOI: https://doi.org/10.1111/jam.14268

Interpretive Summary: The exposure of fecal populations of E. coli that are introduced into agricultural soils, either by contaminated water, application of raw or partially treated manure, or wildlife, subjects these bacteria to a range of ecological stressors not typical of a fecal environment. This study assessed the influence of non-biological and biological factors on the survival of a three-strain cocktail of generic, environmental strains of E. coli in manure-based composts, and compost-amended agricultural soils. In a laboratory experiment, survival of these E. coli strains in sterile and nonsterile compost, soil extracts were determined and results correlated positively with the nutrient content of the extracts. In sterile extracts of compost and soil, E. coli populations increased exponentially at least one million-fold, whereas 100 to 1000-fold increases occurred in non-sterile compost and soil extracts, but populations declined to the detection threshold in unamended soil extracts by 50 h. These results suggest that soil survival of these fecal bacteria, which are typically adapted to high-nutrient fecal environments, may be linked in part to nutrients generated from the extracellular enzyme activity of the indigenous soil organisms that are adapted to low nutrient conditions. In a field experiment, cocktails of these three non-pathogenic, environmental strains of E. coli were sprayed onto plots amended with dairy compost, dairy vermicompost, poultry litter compost, or no compost. Populations of E. coli, soil water potential, soil temperature, extracellular enzyme activity, microbial respiration, phospholipid-fatty acid biomarkers, and the genetic profile of the microbial community were measured over a six-month field season. Results of the field experiment indicate that saturated soils are associated with shifts in community composition, decreased microbial extracellular enzyme activity and respiration, and increased survival of E. coli. Additionally, amendment with ammonium-rich poultry compost resulted in maintenance of high populations of E. coli throughout the field season. Results indicate that nitrogen availability and water potential are strong drivers of E. coli survival in soils. Results of this study on the ecology of E. coli survival in manure-based, compost-amended soils, add to the knowledge base useful to fresh produce growers and industry that are concerned with development and implementation of production practices that support food safety, including appropriate wait times between manure application and harvest of fresh produce crops.

Technical Abstract: This study assessed a variety of abiotic and biotic soil factors that can influence “invasive” copiotrophic coliform bacterial survival in compost-amended agricultural soils. In a laboratory experiment, survival of rifampicin-resistant generic E. coli strains in sterile and nonsterile compost and soil extracts correlated positively with nutrient content of the extracts. The lab experiment showed that E. coli were able to grow well in sterile compost extracts. Conversely, E. coli populations in non-sterile soil extracts survived, but did not grow. These results suggest that survival of copiotrophic organisms, typically adapted to high-nutrient environments, may be linked in part to nutrients generated from the extracellular enzyme activity of the endemic soil oligotrophic organisms. In a field experiment, cocktails of three rifampicin-resistant isolates of non-pathogenic E. coli were sprayed onto plots with dairy compost, dairy vermicompost, poultry litter compost, or no compost. E. coli populations, soil water potential, soil temperature, extracellular enzyme activity, microbial respiration, phospholipid-fatty acid biomarkers, and the genetic profile of the microbial community were measured over a six-month field season. Results of the field experiment suggest that saturated soils are associated with decreases in microbial extracellular enzyme activity and respiration, shifts in community composition, and increased E. coli survival. Additionally, amendment with ammonium-rich poultry compost resulted in maintenance of high populations of E. coli throughout the field season. The results suggest that nitrogen availability and water potential are strong drivers of E. coli survival in soils.