Local and Environmental Reservoirs of Salmonella enterica After Hurricane Florence Flooding

• Published in: Geohealth Vol. 7; no. 11; pp. e2023GH000877 - n/a
• Main Authors: Mao, Yuqing, Zeineldin, Mohamed, Usmani, Moiz, Jutla, Antarpreet, Shisler, Joanna L., Whitaker, Rachel J., Nguyen, Thanh H.
• Format: Journal Article
• Language: English
• Published: United States John Wiley & Sons, Inc 01.11.2023; John Wiley and Sons Inc; American Geophysical Union (AGU)
• Subjects: Agricultural production; Antibiotic resistance; Antibiotics; Bacteria; Chromosomes; Climate change; Drug resistance; Feces; flood; Flooding; Floods; Floodwater; Genetic markers; Genetic testing; Genomes; Geohealth; Hurricanes; Hypotheses; Impacts of Climate Change: Agricultural Health; Impacts of Climate Change: Human Health; long‐read; mobile genetic element; Pathogens; Phylogenetics; Public Health; Salmonella; Swine; Water analysis; Water sampling; whole‐genome sequencing; United States > US; Salmonella; long‐read; whole‐genome sequencing; flood; mobile genetic element
• ISSN: 2471-1403; 2471-1403
• DOI: 10.1029/2023GH000877

In many regions of the world, including the United States, human and animal fecal genetic markers have been found in flood waters. In this study, we use high‐resolution whole genomic sequencing to examine the origin and distribution of Salmonella enterica after the 2018 Hurricane Florence flooding. We specifically asked whether S. enterica isolated from water samples collected near swine farms in North Carolina shortly after Hurricane Florence had evidence of swine origin. To investigate this, we isolated and fully sequenced 18 independent S. enterica strains from 10 locations (five flooded and five unflooded). We found that all strains have extremely similar chromosomes with only five single nucleotide polymorphisms (SNPs) and possessed two plasmids assigned bioinformatically to the incompatibility groups IncFIB and IncFII. The chromosomal core genome and the IncFIB plasmid are most closely related to environmental Salmonella strains isolated previously from the southeastern US. In contrast, the IncFII plasmid was found in environmental S. enterica strains whose genomes were more divergent, suggesting the IncFII plasmid is more promiscuous than the IncFIB type. We identified 65 antibiotic resistance genes (ARGs) in each of our 18 S. enterica isolates. All ARGs were located on the Salmonella chromosome, similar to other previously characterized environmental isolates. All isolates with different SNPs were resistant to a panel of commonly used antibiotics. These results highlight the importance of environmental sources of antibiotic‐resistant S. enterica after extreme flood events. Plain Language Summary Coastal flooding is increasing in frequency due to climate change. It cripples civil infrastructure serving humans and damages many livestock facilities. It is usually assumed that flooding of wastewater, septic systems, and/or livestock manure transmits antibiotic‐resistant bacteria and antibiotic resistance genes to the surrounding environment. However, conclusive identification of the source of the microbial contaminants has not been reported. Moreover, the above assumption rules out environmental reservoirs as a potential source for spread. Here, we report that antibiotic‐resistant Salmonella enterica, isolated from water samples collected near swine farms after Hurricane Florence, were not from animals or manure. Instead, they were from an environmental reservoir. Our findings were based on analyzing chromosomes and plasmids independently and collectively using long‐read high‐fidelity whole‐genome sequences. Knowledge of potential pathogen sources can help mitigate the spread of pathogenic bacteria after hurricanes to minimize the impact of floods on human health. Key Points Salmonella enterica isolated from water samples collected near swine farms after Hurricane Florence were from an environmental reservoir In relation to the chromosome, we also found that one mobile genetic element is more promiscuous than the other Environmental S. enterica were less likely than swine‐associated S. enterica to have antibiotic resistance genes present in plasmids