Local and Environmental Reservoirs of Salmonella enterica After Hurricane Florence Flooding

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....

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Published inGeohealth 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
LanguageEnglish
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
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Abstract 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
AbstractList 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.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.
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. 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
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.
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 after the 2018 Hurricane Florence flooding. We specifically asked whether 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 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 strains isolated previously from the southeastern US. In contrast, the IncFII plasmid was found in environmental 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 isolates. All ARGs were located on the 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 after extreme flood events.
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
Abstract 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.
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. 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. 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
Author Zeineldin, Mohamed
Nguyen, Thanh H.
Usmani, Moiz
Mao, Yuqing
Shisler, Joanna L.
Jutla, Antarpreet
Whitaker, Rachel J.
AuthorAffiliation 1 Department of Civil and Environmental Engineering University of Illinois at Urbana‐Champaign IL Urbana USA
4 Department of Microbiology University of Illinois at Urbana‐Champaign IL Urbana USA
2 Carl R. Woese Institute for Genomic Biology University of Illinois at Urbana‐Champaign IL Urbana USA
3 Engineering School of Sustainable Infrastructure & Environment University of Florida FL Gainesville USA
5 Carle Illinois College of Medicine, University of Illinois at Urbana‐Champaign Urbana IL USA
AuthorAffiliation_xml – name: 4 Department of Microbiology University of Illinois at Urbana‐Champaign IL Urbana USA
– name: 2 Carl R. Woese Institute for Genomic Biology University of Illinois at Urbana‐Champaign IL Urbana USA
– name: 1 Department of Civil and Environmental Engineering University of Illinois at Urbana‐Champaign IL Urbana USA
– name: 3 Engineering School of Sustainable Infrastructure & Environment University of Florida FL Gainesville USA
– name: 5 Carle Illinois College of Medicine, University of Illinois at Urbana‐Champaign Urbana IL USA
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  orcidid: 0000-0002-8191-2348
  surname: Jutla
  fullname: Jutla, Antarpreet
  organization: University of Florida
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  givenname: Joanna L.
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  surname: Shisler
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  surname: Whitaker
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  givenname: Thanh H.
  orcidid: 0000-0002-5461-5233
  surname: Nguyen
  fullname: Nguyen, Thanh H.
  organization: Carle Illinois College of Medicine, University of Illinois at Urbana‐Champaign
BackLink https://www.ncbi.nlm.nih.gov/pubmed/37928215$$D View this record in MEDLINE/PubMed
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Issue 11
Keywords Salmonella
long‐read
whole‐genome sequencing
flood
mobile genetic element
Language English
License Attribution-NonCommercial-NoDerivs
2023 The Authors. GeoHealth published by Wiley Periodicals LLC on behalf of American Geophysical Union.
This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
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Snippet 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...
Abstract 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...
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StartPage e2023GH000877
SubjectTerms 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
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Title Local and Environmental Reservoirs of Salmonella enterica After Hurricane Florence Flooding
URI https://onlinelibrary.wiley.com/doi/abs/10.1029%2F2023GH000877
https://www.ncbi.nlm.nih.gov/pubmed/37928215
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https://pubmed.ncbi.nlm.nih.gov/PMC10624599
https://doaj.org/article/13535fabecc34f088148bd349e86dad0
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