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Whole genome characterization of thermophilic Campylobacter species isolated from dairy manure in small specialty crop farms of Northeast Ohio

INTRODUCTION: With more public interest in consuming locally grown produce, small specialty crop farms (SSCF) are a viable and growing segment of the food production chain in the United States. METHODS: The goal of this study was to investigate the genomic diversity of Campylobacter isolated from da...

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Autores principales: Deblais, Loic, Jang, Hyein, Kauffman, Mike, Gangiredla, Jayanthi, Sawyer, Marianne, Basa, Saritha, Poelstra, Jelmer W., Babu, Uma S., Harrison, Lisa M., Hiett, Kelli L., Balan, Kannan V., Rajashekara, Gireesh
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10071015/
https://www.ncbi.nlm.nih.gov/pubmed/37025625
http://dx.doi.org/10.3389/fmicb.2023.1074548
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author Deblais, Loic
Jang, Hyein
Kauffman, Mike
Gangiredla, Jayanthi
Sawyer, Marianne
Basa, Saritha
Poelstra, Jelmer W.
Babu, Uma S.
Harrison, Lisa M.
Hiett, Kelli L.
Balan, Kannan V.
Rajashekara, Gireesh
author_facet Deblais, Loic
Jang, Hyein
Kauffman, Mike
Gangiredla, Jayanthi
Sawyer, Marianne
Basa, Saritha
Poelstra, Jelmer W.
Babu, Uma S.
Harrison, Lisa M.
Hiett, Kelli L.
Balan, Kannan V.
Rajashekara, Gireesh
author_sort Deblais, Loic
collection PubMed
description INTRODUCTION: With more public interest in consuming locally grown produce, small specialty crop farms (SSCF) are a viable and growing segment of the food production chain in the United States. METHODS: The goal of this study was to investigate the genomic diversity of Campylobacter isolated from dairy manure (n = 69) collected from 10 SSCF in Northeast Ohio between 2018 and 2020. RESULTS: A total of 56 C. jejuni and 13 C. coli isolates were sequenced. Multi-locus sequence typing (MLST) identified 22 sequence types (STs), with ST-922 (18%) and ST-61 (13%) predominant in C. jejuni and ST-829 (62%) and ST-1068 (38%) predominant in C. coli. Interestingly, isolates with similar genomic and gene contents were detected within and between SSCF over time, suggesting that Campylobacter could be transmitted between farms and may persist in a given SSCF over time. Virulence-associated genes (n = 35) involved in the uptake and utilization of potassium and organic compounds (succinate, gluconate, oxoglutarate, and malate) were detected only in the C. jejuni isolates, while 45 genes associated with increased resistance to environmental stresses (capsule production, cell envelope integrity, and iron uptake) were detected only in the C. coli isolates. Campylobacter coli isolates were also sub-divided into two distinct clusters based on the presence of unique prophages (n = 21) or IncQ conjugative plasmid/type-IV secretion system genes (n = 15). Campylobacter coli isolates harbored genes associated with resistance to streptomycin (aadE-Cc; 54%) and quinolone (gyrA-T86I; 77%), while C. jejuni had resistance genes for kanamycin (aph3’-IIIa; 20%). Both species harbored resistance genes associated with β-lactam (especially, blaOXA-193; up to 100%) and tetracycline (tetO; up to 59%). DISCUSSION/CONCLUSION: Our study demonstrated that Campylobacter genome plasticity associated with conjugative transfer might provide resistance to certain antimicrobials and viral infections via the acquisition of protein-encoding genes involved in mechanisms such as ribosomal protection and capsule modification.
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spelling pubmed-100710152023-04-05 Whole genome characterization of thermophilic Campylobacter species isolated from dairy manure in small specialty crop farms of Northeast Ohio Deblais, Loic Jang, Hyein Kauffman, Mike Gangiredla, Jayanthi Sawyer, Marianne Basa, Saritha Poelstra, Jelmer W. Babu, Uma S. Harrison, Lisa M. Hiett, Kelli L. Balan, Kannan V. Rajashekara, Gireesh Front Microbiol Microbiology INTRODUCTION: With more public interest in consuming locally grown produce, small specialty crop farms (SSCF) are a viable and growing segment of the food production chain in the United States. METHODS: The goal of this study was to investigate the genomic diversity of Campylobacter isolated from dairy manure (n = 69) collected from 10 SSCF in Northeast Ohio between 2018 and 2020. RESULTS: A total of 56 C. jejuni and 13 C. coli isolates were sequenced. Multi-locus sequence typing (MLST) identified 22 sequence types (STs), with ST-922 (18%) and ST-61 (13%) predominant in C. jejuni and ST-829 (62%) and ST-1068 (38%) predominant in C. coli. Interestingly, isolates with similar genomic and gene contents were detected within and between SSCF over time, suggesting that Campylobacter could be transmitted between farms and may persist in a given SSCF over time. Virulence-associated genes (n = 35) involved in the uptake and utilization of potassium and organic compounds (succinate, gluconate, oxoglutarate, and malate) were detected only in the C. jejuni isolates, while 45 genes associated with increased resistance to environmental stresses (capsule production, cell envelope integrity, and iron uptake) were detected only in the C. coli isolates. Campylobacter coli isolates were also sub-divided into two distinct clusters based on the presence of unique prophages (n = 21) or IncQ conjugative plasmid/type-IV secretion system genes (n = 15). Campylobacter coli isolates harbored genes associated with resistance to streptomycin (aadE-Cc; 54%) and quinolone (gyrA-T86I; 77%), while C. jejuni had resistance genes for kanamycin (aph3’-IIIa; 20%). Both species harbored resistance genes associated with β-lactam (especially, blaOXA-193; up to 100%) and tetracycline (tetO; up to 59%). DISCUSSION/CONCLUSION: Our study demonstrated that Campylobacter genome plasticity associated with conjugative transfer might provide resistance to certain antimicrobials and viral infections via the acquisition of protein-encoding genes involved in mechanisms such as ribosomal protection and capsule modification. Frontiers Media S.A. 2023-03-21 /pmc/articles/PMC10071015/ /pubmed/37025625 http://dx.doi.org/10.3389/fmicb.2023.1074548 Text en Copyright © 2023 Deblais, Jang, Kauffman, Gangiredla, Sawyer, Basa, Poelstra, Babu, Harrison, Hiett, Balan and Rajashekara. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Deblais, Loic
Jang, Hyein
Kauffman, Mike
Gangiredla, Jayanthi
Sawyer, Marianne
Basa, Saritha
Poelstra, Jelmer W.
Babu, Uma S.
Harrison, Lisa M.
Hiett, Kelli L.
Balan, Kannan V.
Rajashekara, Gireesh
Whole genome characterization of thermophilic Campylobacter species isolated from dairy manure in small specialty crop farms of Northeast Ohio
title Whole genome characterization of thermophilic Campylobacter species isolated from dairy manure in small specialty crop farms of Northeast Ohio
title_full Whole genome characterization of thermophilic Campylobacter species isolated from dairy manure in small specialty crop farms of Northeast Ohio
title_fullStr Whole genome characterization of thermophilic Campylobacter species isolated from dairy manure in small specialty crop farms of Northeast Ohio
title_full_unstemmed Whole genome characterization of thermophilic Campylobacter species isolated from dairy manure in small specialty crop farms of Northeast Ohio
title_short Whole genome characterization of thermophilic Campylobacter species isolated from dairy manure in small specialty crop farms of Northeast Ohio
title_sort whole genome characterization of thermophilic campylobacter species isolated from dairy manure in small specialty crop farms of northeast ohio
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10071015/
https://www.ncbi.nlm.nih.gov/pubmed/37025625
http://dx.doi.org/10.3389/fmicb.2023.1074548
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