Survival of Escherichia coli in Manure-Amended Soils Is Affected by Spatiotemporal, Agricultural, and Weather Factors in the Mid-Atlantic United States

Abstract

Untreated biological soil amendments of animal origin (BSAAO), such as manure, are commonly used to fertilize soils for growing fruit and vegetable crops and can contain enteric bacterial foodborne pathogens. Little is known about the comparative longitudinal survival of pathogens in agricultural fields containing different types of BSAAO, and field data may be useful to determine intervals between manure application and harvest of produce intended for human consumption to minimize foodborne illness. This study generated 324 survival profiles from 12 different field trials at three different sites (UMES, PA, and BARC) in the Mid-Atlantic United States from 2011 to 2015 of inoculated nonpathogenic Escherichia coli (gEc) and attenuated O157 E. coli (attO157) in soils which were unamended (UN) or amended with untreated poultry litter (PL), horse manure (HM), or dairy manure solids (DMS) or liquids (DML). Site, season, inoculum level (low/high), amendment type, management (organic/conventional), and depth (surface/tilled) all significantly (P < 0.0001) influenced survival duration (dpi100mort). Spatiotemporal factors (site, year, and season) in which the field trial was conducted influenced survival durations of gEc and attO157 to a greater extent than weather effects (average daily temperature and rainfall). Initial soil moisture content was the individual factor that accounted for the greatest percentage of variability in survival duration. PL supported greater survival durations of gEc and attO157, followed by HM, UN, and DMS in amended soils. The majority of survival profiles for gEc and attO157 which survived for more than 90 days came from a specific year (i.e., 2013). The effect of management and depth on dpi100mort were dependent on the amendment type evaluated. IMPORTANCE Current language in the Food Safety Modernization Act Produce Safety Rule states no objection to a 90- or 120-day interval between application of untreated BSAAO and harvest of crops to minimize transfer of pathogens to produce intended for human consumption with the intent to limit potential cases of foodborne illness. This regional multiple season, multiple location field trial determined survival durations of Escherichia coli in soils amended with manure to determine whether this interval is appropriate. Spatiotemporal factors influence survival durations of E. coli more than amendment type, total amount of E. coli present, organic or conventional soil management, and depth of manure application. Overall, these data show poultry litter may support extended survival of E. coli compared to horse manure or dairy manure, but spatiotemporal factors like site and season may have more influence than manure type in supporting survival of E. coli beyond 90 days in amended soils in the Mid-Atlantic United States.

Composts of poultry litter or dairy manure differentially affect survival of enteric bacteria in fields with spinach

“…Greater survival of these E. coli strains in soils amended with poultry litter than dairy manure-based soil amendments was observed previously in a greenhouse setting ) and in field trials conducted in the Mid-Atlantic United States (Sharma et al 2019). Soil amended with poultry compost contained more NH 4 -N and a distinct composition of microbial taxa compared to dairy compost or no compost.…”

“…) and in field trials conducted in the Mid‐Atlantic United States (Sharma et al . ). Soil amended with poultry compost contained more NH 4 ‐N and a distinct composition of microbial taxa compared to dairy compost or no compost.…”

“…As a single factor, initial soil moisture content (measured gravimetrically) accounted for the greatest proportion of variability in E. coli survival durations in manure‐amended soils, with survival duration greater in initially drier soils (Sharma et al . ). In the current study, soil moisture (water potential) was monitored throughout the duration of the study rather than solely at the outset, and different amendment (manure vs compost), soil types and climatic conditions may have led to different relationships between moisture content and E. coli survival between the current study and previous ones.…”

“…A three-strain inoculum of rifampicin-resistant nonpathogenic E. coli (TVS 353,354 and 355) were used to distinguish them from indigenous microbes in composts or soil (hereafter referenced as 'indigenous'). These strains were isolated from agricultural environments and have been used previously in greenhouse and field studies involving soil amendments (Reynnells et al 2014;Sharma et al 2019). Each E. coli strain was grown in tryptic soy broth with 80 lg ml À1 rifampicin (TSBR) and adjusted to a final population of 1Á67 9 10 5 CFU per ml.…”

Assessment of Biological Soil Amendments of Animal Origin Use, Research Needs, and Extension Opportunities in Organic Production

“…However, there are currently no safety regulations governing wait times for use of raw manure in conventional agriculture. Moreover, guidelines and proposed rules by organizations and federal agencies in the United States often overlap or are based on inadequate scientific data to minimize the risk of microbial contamination and how agricultural practices may affect contamination and survival (Sharma and Reynnells, 2016;Pires et al, 2018;Sharma et al, 2019).…”