Agricultural fertilization with poultry manure results in persistent environmental contamination with the pathogen Clostridioides difficile

Abstract

During a field experiment applying broiler manure for fertilization of agricultural land, we detected viable Clostridioides (also known as Clostridium) difficile in broiler faeces, manure, dust and fertilized soil. A large diversity of toxigenic C. difficile isolates was recovered, including PCR ribotypes common from human disease. Genomic relatedness of C. difficile isolates from dust and from soil, recovered more than 2 years after fertilization, traced their origins to the specific chicken farm that had delivered the manure. We present evidence of long-term contamination of agricultural soil with manure-derived C. difficile and demonstrate the potential for airborne dispersal of C. difficile through dust emissions during manure application. Clostridioides genome sequences virtually identical to those from manure had been recovered from chicken meat and from human infections in previous studies, suggesting broiler-associated C. difficile are capable of zoonotic transmission.

Bacterial genome sequencing tracks the housefly‐associated dispersal of fluoroquinolone‐ and cephalosporin‐resistant Escherichia coli from a pig farm

“…This might suggest that transmission of E. coli from the pig farm to humans has not occurred frequently, or at least has not caused clinical disease in humans frequently (as most genomesequenced E. coli originate from infections rather than symptom-free colonization). This result is in contrast to our previous study, which used EnteroBase to identify near-identical genomes among Clostridioides difficile isolates originating from chicken manure, retail chicken meat, and human infections from independent previous investigations, even though the database for Clostridioides at the time was 10 times smaller than the current Escherichia database (Frentrup et al, 2021). A more thorough assessment of pathogen spread from the farm to human residents would require simultaneous, extensive sampling of E. coli genomes from livestock and humans in the same area.…”

Comparative genomic and transmission analysis of Clostridioides difficile between environmental, animal, and clinical sources in China

“…This suggests that no significant genomic differences exist between C. difficile strains from farmers, soil, and pigs. Frentrup et al found that RT001 strains isolated from broiler manure were genetic associated with human isolates [ 44 ]. Werner et al confirmed that RT046 strains isolated from piglets and environment were closely related with human isolates [ 15 ].…”

Microbiome diversity and zoonotic bacterial pathogen prevalence in Peromyscus mice from agricultural landscapes and synanthropic habitat

“…As such, the low read counts (read count <200) et al, 2021). In agricultural settings, manure used as fertilizer may serve as a source of environmental contamination for faecal-oral pathogens such as C. difficile (Frentrup et al, 2021) which could provide a transmission route to rodents and other wildlife.…”

“…We predicted that microbiome diversity would be lower in the agricultural landscape and synanthropic habitats compared to the undeveloped landscape and forest habitats due to lower diversity of food resources (Amato et al., 2013; Fuirst et al., 2018). We predicted that the agricultural landscape would have a higher prevalence and diversity of pathogenic bacteria since the area is dominated by crop fields and human habitation and thus increased exposure to manure as fertilizer (Frentrup et al., 2021), wastewater and runoff (Graczyk et al., 2009; Ramey & Ahlstrom, 2019), and trash (Sugden et al., 2020), whereas we predicted that the undeveloped landscape would have lower pathogen prevalence because the surrounding area is largely forested with little anthropogenic development. Characterizing rodent microbiomes across landscape and habitat types is important for quantifying the risk of rodent‐borne zoonotic pathogen spillover in anthropogenic environments and understanding how microbiome shifts associated with synanthropy may influence pathogen prevalence.…”