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Genomic Comparison of Campylobacter spp. and Their Potential for Zoonotic Transmission between Birds, Primates, and Livestock
Campylobacter is the leading cause of human gastroenteritis worldwide. Wild birds, including American crows, are abundant in urban, suburban, and agricultural settings and are likely zoonotic vectors of Campylobacter Their proximity to humans and livestock increases the potential spreading of Campyl...
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Published in: | Applied and environmental microbiology 2016-12, Vol.82 (24), p.7165-7175 |
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description | Campylobacter is the leading cause of human gastroenteritis worldwide. Wild birds, including American crows, are abundant in urban, suburban, and agricultural settings and are likely zoonotic vectors of Campylobacter Their proximity to humans and livestock increases the potential spreading of Campylobacter via crows between the environment, livestock, and humans. However, no studies have definitively demonstrated that crows are a vector for pathogenic Campylobacter We used genomics to evaluate the zoonotic and pathogenic potential of Campylobacter from crows to other animals with 184 isolates obtained from crows, chickens, cows, sheep, goats, humans, and nonhuman primates. Whole-genome analysis uncovered two distinct clades of Campylobacter jejuni genotypes; the first contained genotypes found only in crows, while a second genotype contained "generalist" genomes that were isolated from multiple host species, including isolates implicated in human disease, primate gastroenteritis, and livestock abortion. Two major β-lactamase genes were observed frequently in these genomes (oxa-184, 55%, and oxa-61, 29%), where oxa-184 was associated only with crows and oxa-61 was associated with generalists. Mutations in gyrA, indicative of fluoroquinolone resistance, were observed in 14% of the isolates. Tetracycline resistance (tetO) was present in 22% of the isolates, yet it occurred in 91% of the abortion isolates. Virulence genes were distributed throughout the genomes; however, cdtC alleles recapitulated the crow-only and generalist clades. A specific cdtC allele was associated with abortion in livestock and was concomitant with tetO These findings indicate that crows harboring a generalist C. jejuni genotype may act as a vector for the zoonotic transmission of Campylobacter IMPORTANCE: This study examined the link between public health and the genomic variation of Campylobacter in relation to disease in humans, primates, and livestock. Use of large-scale whole-genome sequencing enabled population-level assessment to find new genes that are linked to livestock disease. With 184 Campylobacter genomes, we assessed virulence traits, antibiotic resistance susceptibility, and the potential for zoonotic transfer to observe that there is a "generalist" genotype that may move between host species. |
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A.</contributor><creatorcontrib>Weis, Allison M ; Storey, Dylan B ; Taff, Conor C ; Townsend, Andrea K ; Huang, Bihua C ; Kong, Nguyet T ; Clothier, Kristin A ; Spinner, Abigail ; Byrne, Barbara A ; Weimer, Bart C ; Elkins, C. A.</creatorcontrib><description>Campylobacter is the leading cause of human gastroenteritis worldwide. Wild birds, including American crows, are abundant in urban, suburban, and agricultural settings and are likely zoonotic vectors of Campylobacter Their proximity to humans and livestock increases the potential spreading of Campylobacter via crows between the environment, livestock, and humans. However, no studies have definitively demonstrated that crows are a vector for pathogenic Campylobacter We used genomics to evaluate the zoonotic and pathogenic potential of Campylobacter from crows to other animals with 184 isolates obtained from crows, chickens, cows, sheep, goats, humans, and nonhuman primates. Whole-genome analysis uncovered two distinct clades of Campylobacter jejuni genotypes; the first contained genotypes found only in crows, while a second genotype contained "generalist" genomes that were isolated from multiple host species, including isolates implicated in human disease, primate gastroenteritis, and livestock abortion. Two major β-lactamase genes were observed frequently in these genomes (oxa-184, 55%, and oxa-61, 29%), where oxa-184 was associated only with crows and oxa-61 was associated with generalists. Mutations in gyrA, indicative of fluoroquinolone resistance, were observed in 14% of the isolates. Tetracycline resistance (tetO) was present in 22% of the isolates, yet it occurred in 91% of the abortion isolates. Virulence genes were distributed throughout the genomes; however, cdtC alleles recapitulated the crow-only and generalist clades. A specific cdtC allele was associated with abortion in livestock and was concomitant with tetO These findings indicate that crows harboring a generalist C. jejuni genotype may act as a vector for the zoonotic transmission of Campylobacter IMPORTANCE: This study examined the link between public health and the genomic variation of Campylobacter in relation to disease in humans, primates, and livestock. Use of large-scale whole-genome sequencing enabled population-level assessment to find new genes that are linked to livestock disease. With 184 Campylobacter genomes, we assessed virulence traits, antibiotic resistance susceptibility, and the potential for zoonotic transfer to observe that there is a "generalist" genotype that may move between host species.</description><identifier>ISSN: 0099-2240</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/AEM.01746-16</identifier><identifier>PMID: 27736787</identifier><identifier>CODEN: AEMIDF</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Animals ; Animals, Wild - microbiology ; Bird Diseases - microbiology ; Bird Diseases - transmission ; Birds ; Birds - microbiology ; Campylobacter - classification ; Campylobacter - genetics ; Campylobacter - isolation & purification ; Campylobacter - physiology ; Campylobacter Infections - microbiology ; Campylobacter Infections - transmission ; Campylobacter Infections - veterinary ; Cattle ; Disease transmission ; Gastrointestinal diseases ; Genome, Bacterial ; Genomics ; Genotype ; Genotype & phenotype ; Gram-negative bacteria ; Humans ; Livestock ; Livestock - microbiology ; Phylogeny ; Primate Diseases - microbiology ; Primate Diseases - transmission ; Primates - microbiology ; Public and Environmental Health Microbiology ; Sheep ; Zoonoses - microbiology ; Zoonoses - transmission</subject><ispartof>Applied and environmental microbiology, 2016-12, Vol.82 (24), p.7165-7175</ispartof><rights>Copyright © 2016, American Society for Microbiology. All Rights Reserved.</rights><rights>Copyright American Society for Microbiology Dec 2016</rights><rights>Copyright © 2016, American Society for Microbiology. All Rights Reserved. 2016 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c455t-701d488f7214383c1afe3733026bed3edf19449592aafcfb6313963274b1c1aa3</citedby><cites>FETCH-LOGICAL-c455t-701d488f7214383c1afe3733026bed3edf19449592aafcfb6313963274b1c1aa3</cites><orcidid>0000-0002-7471-1978</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5118927/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5118927/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,3188,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27736787$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Elkins, C. A.</contributor><creatorcontrib>Weis, Allison M</creatorcontrib><creatorcontrib>Storey, Dylan B</creatorcontrib><creatorcontrib>Taff, Conor C</creatorcontrib><creatorcontrib>Townsend, Andrea K</creatorcontrib><creatorcontrib>Huang, Bihua C</creatorcontrib><creatorcontrib>Kong, Nguyet T</creatorcontrib><creatorcontrib>Clothier, Kristin A</creatorcontrib><creatorcontrib>Spinner, Abigail</creatorcontrib><creatorcontrib>Byrne, Barbara A</creatorcontrib><creatorcontrib>Weimer, Bart C</creatorcontrib><title>Genomic Comparison of Campylobacter spp. and Their Potential for Zoonotic Transmission between Birds, Primates, and Livestock</title><title>Applied and environmental microbiology</title><addtitle>Appl Environ Microbiol</addtitle><description>Campylobacter is the leading cause of human gastroenteritis worldwide. Wild birds, including American crows, are abundant in urban, suburban, and agricultural settings and are likely zoonotic vectors of Campylobacter Their proximity to humans and livestock increases the potential spreading of Campylobacter via crows between the environment, livestock, and humans. However, no studies have definitively demonstrated that crows are a vector for pathogenic Campylobacter We used genomics to evaluate the zoonotic and pathogenic potential of Campylobacter from crows to other animals with 184 isolates obtained from crows, chickens, cows, sheep, goats, humans, and nonhuman primates. Whole-genome analysis uncovered two distinct clades of Campylobacter jejuni genotypes; the first contained genotypes found only in crows, while a second genotype contained "generalist" genomes that were isolated from multiple host species, including isolates implicated in human disease, primate gastroenteritis, and livestock abortion. Two major β-lactamase genes were observed frequently in these genomes (oxa-184, 55%, and oxa-61, 29%), where oxa-184 was associated only with crows and oxa-61 was associated with generalists. Mutations in gyrA, indicative of fluoroquinolone resistance, were observed in 14% of the isolates. Tetracycline resistance (tetO) was present in 22% of the isolates, yet it occurred in 91% of the abortion isolates. Virulence genes were distributed throughout the genomes; however, cdtC alleles recapitulated the crow-only and generalist clades. A specific cdtC allele was associated with abortion in livestock and was concomitant with tetO These findings indicate that crows harboring a generalist C. jejuni genotype may act as a vector for the zoonotic transmission of Campylobacter IMPORTANCE: This study examined the link between public health and the genomic variation of Campylobacter in relation to disease in humans, primates, and livestock. Use of large-scale whole-genome sequencing enabled population-level assessment to find new genes that are linked to livestock disease. 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A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genomic Comparison of Campylobacter spp. and Their Potential for Zoonotic Transmission between Birds, Primates, and Livestock</atitle><jtitle>Applied and environmental microbiology</jtitle><addtitle>Appl Environ Microbiol</addtitle><date>2016-12-15</date><risdate>2016</risdate><volume>82</volume><issue>24</issue><spage>7165</spage><epage>7175</epage><pages>7165-7175</pages><issn>0099-2240</issn><eissn>1098-5336</eissn><coden>AEMIDF</coden><abstract>Campylobacter is the leading cause of human gastroenteritis worldwide. Wild birds, including American crows, are abundant in urban, suburban, and agricultural settings and are likely zoonotic vectors of Campylobacter Their proximity to humans and livestock increases the potential spreading of Campylobacter via crows between the environment, livestock, and humans. However, no studies have definitively demonstrated that crows are a vector for pathogenic Campylobacter We used genomics to evaluate the zoonotic and pathogenic potential of Campylobacter from crows to other animals with 184 isolates obtained from crows, chickens, cows, sheep, goats, humans, and nonhuman primates. Whole-genome analysis uncovered two distinct clades of Campylobacter jejuni genotypes; the first contained genotypes found only in crows, while a second genotype contained "generalist" genomes that were isolated from multiple host species, including isolates implicated in human disease, primate gastroenteritis, and livestock abortion. Two major β-lactamase genes were observed frequently in these genomes (oxa-184, 55%, and oxa-61, 29%), where oxa-184 was associated only with crows and oxa-61 was associated with generalists. Mutations in gyrA, indicative of fluoroquinolone resistance, were observed in 14% of the isolates. Tetracycline resistance (tetO) was present in 22% of the isolates, yet it occurred in 91% of the abortion isolates. Virulence genes were distributed throughout the genomes; however, cdtC alleles recapitulated the crow-only and generalist clades. A specific cdtC allele was associated with abortion in livestock and was concomitant with tetO These findings indicate that crows harboring a generalist C. jejuni genotype may act as a vector for the zoonotic transmission of Campylobacter IMPORTANCE: This study examined the link between public health and the genomic variation of Campylobacter in relation to disease in humans, primates, and livestock. Use of large-scale whole-genome sequencing enabled population-level assessment to find new genes that are linked to livestock disease. With 184 Campylobacter genomes, we assessed virulence traits, antibiotic resistance susceptibility, and the potential for zoonotic transfer to observe that there is a "generalist" genotype that may move between host species.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>27736787</pmid><doi>10.1128/AEM.01746-16</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-7471-1978</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Animals, Wild - microbiology Bird Diseases - microbiology Bird Diseases - transmission Birds Birds - microbiology Campylobacter - classification Campylobacter - genetics Campylobacter - isolation & purification Campylobacter - physiology Campylobacter Infections - microbiology Campylobacter Infections - transmission Campylobacter Infections - veterinary Cattle Disease transmission Gastrointestinal diseases Genome, Bacterial Genomics Genotype Genotype & phenotype Gram-negative bacteria Humans Livestock Livestock - microbiology Phylogeny Primate Diseases - microbiology Primate Diseases - transmission Primates - microbiology Public and Environmental Health Microbiology Sheep Zoonoses - microbiology Zoonoses - transmission |
title | Genomic Comparison of Campylobacter spp. and Their Potential for Zoonotic Transmission between Birds, Primates, and Livestock |
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