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

IntroductionWith 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.MethodsThe goal of this study was to investigate the genomic diversity of Campylobacter isolated from dairy m...

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Main Authors: Loic Deblais, Hyein Jang, Mike Kauffman, Jayanthi Gangiredla, Marianne Sawyer, Saritha Basa, Jelmer W. Poelstra, Uma S. Babu, Lisa M. Harrison, Kelli L. Hiett, Kannan V. Balan, Gireesh Rajashekara
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-03-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1074548/full
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author Loic Deblais
Hyein Jang
Mike Kauffman
Jayanthi Gangiredla
Marianne Sawyer
Saritha Basa
Jelmer W. Poelstra
Uma S. Babu
Lisa M. Harrison
Kelli L. Hiett
Kannan V. Balan
Gireesh Rajashekara
author_facet Loic Deblais
Hyein Jang
Mike Kauffman
Jayanthi Gangiredla
Marianne Sawyer
Saritha Basa
Jelmer W. Poelstra
Uma S. Babu
Lisa M. Harrison
Kelli L. Hiett
Kannan V. Balan
Gireesh Rajashekara
author_sort Loic Deblais
collection DOAJ
description IntroductionWith 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.MethodsThe 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.ResultsA 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/ConclusionOur 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 doaj.art-8a83bed36bc5472eb79797da26195c542023-03-21T05:39:11ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-03-011410.3389/fmicb.2023.10745481074548Whole genome characterization of thermophilic Campylobacter species isolated from dairy manure in small specialty crop farms of Northeast OhioLoic Deblais0Hyein Jang1Mike Kauffman2Jayanthi Gangiredla3Marianne Sawyer4Saritha Basa5Jelmer W. Poelstra6Uma S. Babu7Lisa M. Harrison8Kelli L. Hiett9Kannan V. Balan10Gireesh Rajashekara11Department of Animal Sciences, Center for Food Animal Health, The Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH, United StatesCenter for Food Safety and Applied Nutrition (CFSAN), Office of Applied Research and Safety Assessment (OARSA), U.S. Food and Drug Administration, Laurel, MD, United StatesDepartment of Animal Sciences, Center for Food Animal Health, The Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH, United StatesCenter for Food Safety and Applied Nutrition (CFSAN), Office of Applied Research and Safety Assessment (OARSA), U.S. Food and Drug Administration, Laurel, MD, United StatesCenter for Food Safety and Applied Nutrition (CFSAN), Office of Applied Research and Safety Assessment (OARSA), U.S. Food and Drug Administration, Laurel, MD, United StatesCenter for Food Safety and Applied Nutrition (CFSAN), Office of Applied Research and Safety Assessment (OARSA), U.S. Food and Drug Administration, Laurel, MD, United StatesMolecular and Cellular Imaging Center, The Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH, United StatesCenter for Food Safety and Applied Nutrition (CFSAN), Office of Applied Research and Safety Assessment (OARSA), U.S. Food and Drug Administration, Laurel, MD, United StatesCenter for Food Safety and Applied Nutrition (CFSAN), Office of Applied Research and Safety Assessment (OARSA), U.S. Food and Drug Administration, Laurel, MD, United StatesCenter for Food Safety and Applied Nutrition (CFSAN), Office of Applied Research and Safety Assessment (OARSA), U.S. Food and Drug Administration, Laurel, MD, United StatesCenter for Food Safety and Applied Nutrition (CFSAN), Office of Applied Research and Safety Assessment (OARSA), U.S. Food and Drug Administration, Laurel, MD, United StatesDepartment of Animal Sciences, Center for Food Animal Health, The Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH, United StatesIntroductionWith 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.MethodsThe 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.ResultsA 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/ConclusionOur 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.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1074548/fullCampylobacter jejuniCampylobacter coliwhole genome sequencingdairy manuresmall specialty crop farmresistome
spellingShingle Loic Deblais
Hyein Jang
Mike Kauffman
Jayanthi Gangiredla
Marianne Sawyer
Saritha Basa
Jelmer W. Poelstra
Uma S. Babu
Lisa M. Harrison
Kelli L. Hiett
Kannan V. Balan
Gireesh Rajashekara
Whole genome characterization of thermophilic Campylobacter species isolated from dairy manure in small specialty crop farms of Northeast Ohio
Frontiers in Microbiology
Campylobacter jejuni
Campylobacter coli
whole genome sequencing
dairy manure
small specialty crop farm
resistome
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 Campylobacter jejuni
Campylobacter coli
whole genome sequencing
dairy manure
small specialty crop farm
resistome
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1074548/full
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