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Effects of Eimeria tenella infection on chicken caecal microbiome diversity, exploring variation associated with severity of pathology
Eimeria species cause the intestinal disease coccidiosis, most notably in poultry. While the direct impact of coccidiosis on animal health and welfare is clear, its influence on the enteric microbiota and by-stander effects on chicken health and production remains largely unknown, with the possible...
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Published in: | PloS one 2017-09, Vol.12 (9), p.e0184890-e0184890 |
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description | Eimeria species cause the intestinal disease coccidiosis, most notably in poultry. While the direct impact of coccidiosis on animal health and welfare is clear, its influence on the enteric microbiota and by-stander effects on chicken health and production remains largely unknown, with the possible exception of Clostridium perfringens (necrotic enteritis). This study evaluated the composition and structure of the caecal microbiome in the presence or absence of a defined Eimeria tenella challenge infection in Cobb500 broiler chickens using 16S rRNA amplicon sequencing. The severity of clinical coccidiosis in individual chickens was quantified by caecal lesion scoring and microbial changes associated with different lesion scores identified. Following E. tenella infection the diversity of taxa within the caecal microbiome remained largely stable. However, infection induced significant changes in the abundance of some microbial taxa. The greatest changes were detected in birds displaying severe caecal pathology; taxa belonging to the order Enterobacteriaceae were increased, while taxa from Bacillales and Lactobacillales were decreased with the changes correlated with lesion severity. Significantly different profiles were also detected in infected birds which remained asymptomatic (lesion score 0), with taxa belonging to the genera Bacteroides decreased and Lactobacillus increased. Many differential taxa from the order Clostridiales were identified, with some increasing and others decreasing in abundance in Eimeria-infected animals. The results support the view that caecal microbiome dysbiosis associated with Eimeria infection contributes to disease pathology, and could be a target for intervention to mitigate the impact of coccidiosis on poultry productivity and welfare. This work highlights that E. tenella infection has a significant impact on the abundance of some caecal bacteria with notable differences detected between lesion score categories emphasising the importance of accounting for differences in caecal lesions when investigating the relationship between E. tenella and the poultry intestinal microbiome. |
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While the direct impact of coccidiosis on animal health and welfare is clear, its influence on the enteric microbiota and by-stander effects on chicken health and production remains largely unknown, with the possible exception of Clostridium perfringens (necrotic enteritis). This study evaluated the composition and structure of the caecal microbiome in the presence or absence of a defined Eimeria tenella challenge infection in Cobb500 broiler chickens using 16S rRNA amplicon sequencing. The severity of clinical coccidiosis in individual chickens was quantified by caecal lesion scoring and microbial changes associated with different lesion scores identified. Following E. tenella infection the diversity of taxa within the caecal microbiome remained largely stable. However, infection induced significant changes in the abundance of some microbial taxa. The greatest changes were detected in birds displaying severe caecal pathology; taxa belonging to the order Enterobacteriaceae were increased, while taxa from Bacillales and Lactobacillales were decreased with the changes correlated with lesion severity. Significantly different profiles were also detected in infected birds which remained asymptomatic (lesion score 0), with taxa belonging to the genera Bacteroides decreased and Lactobacillus increased. Many differential taxa from the order Clostridiales were identified, with some increasing and others decreasing in abundance in Eimeria-infected animals. The results support the view that caecal microbiome dysbiosis associated with Eimeria infection contributes to disease pathology, and could be a target for intervention to mitigate the impact of coccidiosis on poultry productivity and welfare. This work highlights that E. tenella infection has a significant impact on the abundance of some caecal bacteria with notable differences detected between lesion score categories emphasising the importance of accounting for differences in caecal lesions when investigating the relationship between E. tenella and the poultry intestinal microbiome.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0184890</identifier><identifier>PMID: 28934262</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abundance ; Age ; Animal health ; Animals ; Bacteria ; Biodiversity ; Biology and Life Sciences ; Bird Diseases - microbiology ; Bird Diseases - pathology ; Birds ; Broilers (Chickens) ; Causes of ; Cecum - microbiology ; Cecum - pathology ; Change detection ; Chickens ; Chickens - microbiology ; Coccidiosis ; Coccidiosis - microbiology ; Coccidiosis - pathology ; Coccidiosis - veterinary ; Development and progression ; Diseases and pests ; Drug resistance ; Dysbacteriosis ; E coli ; Eimeria tenella ; Enteritis ; Gastrointestinal Microbiome - genetics ; Genotype & phenotype ; Infections ; Inflammatory bowel disease ; Intervention ; Intestine ; Lesions ; Medicine and Health Sciences ; Microbiota (Symbiotic organisms) ; Microorganisms ; Parasites ; Pathology ; Phylogeny ; Physiological aspects ; Population ; Poultry ; Probiotics ; Random Allocation ; RNA, Ribosomal, 16S - genetics ; rRNA 16S ; Salmonella ; Sequence Analysis, DNA ; Severity of Illness Index ; Species diversity ; Taxa ; Veterinary colleges</subject><ispartof>PloS one, 2017-09, Vol.12 (9), p.e0184890-e0184890</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Macdonald et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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While the direct impact of coccidiosis on animal health and welfare is clear, its influence on the enteric microbiota and by-stander effects on chicken health and production remains largely unknown, with the possible exception of Clostridium perfringens (necrotic enteritis). This study evaluated the composition and structure of the caecal microbiome in the presence or absence of a defined Eimeria tenella challenge infection in Cobb500 broiler chickens using 16S rRNA amplicon sequencing. The severity of clinical coccidiosis in individual chickens was quantified by caecal lesion scoring and microbial changes associated with different lesion scores identified. Following E. tenella infection the diversity of taxa within the caecal microbiome remained largely stable. However, infection induced significant changes in the abundance of some microbial taxa. The greatest changes were detected in birds displaying severe caecal pathology; taxa belonging to the order Enterobacteriaceae were increased, while taxa from Bacillales and Lactobacillales were decreased with the changes correlated with lesion severity. Significantly different profiles were also detected in infected birds which remained asymptomatic (lesion score 0), with taxa belonging to the genera Bacteroides decreased and Lactobacillus increased. Many differential taxa from the order Clostridiales were identified, with some increasing and others decreasing in abundance in Eimeria-infected animals. The results support the view that caecal microbiome dysbiosis associated with Eimeria infection contributes to disease pathology, and could be a target for intervention to mitigate the impact of coccidiosis on poultry productivity and welfare. 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pathology</subject><subject>Coccidiosis - veterinary</subject><subject>Development and progression</subject><subject>Diseases and pests</subject><subject>Drug resistance</subject><subject>Dysbacteriosis</subject><subject>E coli</subject><subject>Eimeria tenella</subject><subject>Enteritis</subject><subject>Gastrointestinal Microbiome - genetics</subject><subject>Genotype & phenotype</subject><subject>Infections</subject><subject>Inflammatory bowel disease</subject><subject>Intervention</subject><subject>Intestine</subject><subject>Lesions</subject><subject>Medicine and Health Sciences</subject><subject>Microbiota (Symbiotic organisms)</subject><subject>Microorganisms</subject><subject>Parasites</subject><subject>Pathology</subject><subject>Phylogeny</subject><subject>Physiological aspects</subject><subject>Population</subject><subject>Poultry</subject><subject>Probiotics</subject><subject>Random Allocation</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>rRNA 16S</subject><subject>Salmonella</subject><subject>Sequence Analysis, DNA</subject><subject>Severity of Illness Index</subject><subject>Species diversity</subject><subject>Taxa</subject><subject>Veterinary colleges</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk22L1DAQx4so3nn6DUQLgii4ax7atHkjHMeqCwcHPr0NaTptc7bNmqTr7Rfwc5vu9o6t3AtpIUPym_9MZjJR9ByjJaYZfn9tBtvLdrkxPSwRzpOcowfRKeaULBhB9OGRfRI9ce4aoZTmjD2OTkjOaUIYOY3-rKoKlHexqeKV7sBqGXvooW1lrPvxSJs-Dr9qtPoJYZWgZBt3WllTaNNBXOotWKf97l0MN5vWWN3X8VYGpb2vdM6oYEMZ_9a-iR0EPNBjxI30jWlNvXsaPapk6-DZtJ5F3z-uvl18XlxefVpfnF8uFOPELzLFJRSY8FyhBCdVAamCiueVYhnFPMuLgpV5SRTNspB7WvAMcsIpcA4FSxN6Fr086IY8nZhK6ATmCaYJZmQk1geiNPJabKzupN0JI7XYbxhbC2m9Vi0IRgGoRAVKCB6rz1mwM0apUopksgxaH6ZoQ9FBqaD3VrYz0flJrxtRm61IGcoJHZN5MwlY82sA50WnnRqb04MZ9nkTluPQ1oC--ge9_3YTVctwgdBgE-KqUVScpyjN0jTBKFDLe6jwlRD6Ht5bpcP-zOHtzCEwHm58LQfnxPrrl_9nr37M2ddHbAOy9Y0z7TA-LDcHkwMYXqVzFqq7ImMkxnG5rYYYx0VM4xLcXhw36M7pdj7oX6aIEhY</recordid><startdate>20170921</startdate><enddate>20170921</enddate><creator>Macdonald, Sarah E</creator><creator>Nolan, Matthew J</creator><creator>Harman, Kimberley</creator><creator>Boulton, Kay</creator><creator>Hume, David A</creator><creator>Tomley, Fiona M</creator><creator>Stabler, Richard A</creator><creator>Blake, Damer P</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-4710-0191</orcidid></search><sort><creationdate>20170921</creationdate><title>Effects of Eimeria tenella infection on chicken caecal microbiome diversity, exploring variation associated with severity of pathology</title><author>Macdonald, Sarah E ; Nolan, Matthew J ; Harman, Kimberley ; Boulton, Kay ; Hume, David A ; Tomley, Fiona M ; Stabler, Richard A ; Blake, Damer P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-7c9aeb1298c0414fbe5cef98fc6731978bb6d8d2c377fec5b97e8293e99eb6543</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Abundance</topic><topic>Age</topic><topic>Animal health</topic><topic>Animals</topic><topic>Bacteria</topic><topic>Biodiversity</topic><topic>Biology and Life Sciences</topic><topic>Bird Diseases - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Macdonald, Sarah E</au><au>Nolan, Matthew J</au><au>Harman, Kimberley</au><au>Boulton, Kay</au><au>Hume, David A</au><au>Tomley, Fiona M</au><au>Stabler, Richard A</au><au>Blake, Damer P</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Effects of Eimeria tenella infection on chicken caecal microbiome diversity, exploring variation associated with severity of pathology</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-09-21</date><risdate>2017</risdate><volume>12</volume><issue>9</issue><spage>e0184890</spage><epage>e0184890</epage><pages>e0184890-e0184890</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Competing Interests: The authors have declared that no competing interests exist.</notes><abstract>Eimeria species cause the intestinal disease coccidiosis, most notably in poultry. While the direct impact of coccidiosis on animal health and welfare is clear, its influence on the enteric microbiota and by-stander effects on chicken health and production remains largely unknown, with the possible exception of Clostridium perfringens (necrotic enteritis). This study evaluated the composition and structure of the caecal microbiome in the presence or absence of a defined Eimeria tenella challenge infection in Cobb500 broiler chickens using 16S rRNA amplicon sequencing. The severity of clinical coccidiosis in individual chickens was quantified by caecal lesion scoring and microbial changes associated with different lesion scores identified. Following E. tenella infection the diversity of taxa within the caecal microbiome remained largely stable. However, infection induced significant changes in the abundance of some microbial taxa. The greatest changes were detected in birds displaying severe caecal pathology; taxa belonging to the order Enterobacteriaceae were increased, while taxa from Bacillales and Lactobacillales were decreased with the changes correlated with lesion severity. Significantly different profiles were also detected in infected birds which remained asymptomatic (lesion score 0), with taxa belonging to the genera Bacteroides decreased and Lactobacillus increased. Many differential taxa from the order Clostridiales were identified, with some increasing and others decreasing in abundance in Eimeria-infected animals. The results support the view that caecal microbiome dysbiosis associated with Eimeria infection contributes to disease pathology, and could be a target for intervention to mitigate the impact of coccidiosis on poultry productivity and welfare. This work highlights that E. tenella infection has a significant impact on the abundance of some caecal bacteria with notable differences detected between lesion score categories emphasising the importance of accounting for differences in caecal lesions when investigating the relationship between E. tenella and the poultry intestinal microbiome.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28934262</pmid><doi>10.1371/journal.pone.0184890</doi><tpages>e0184890</tpages><orcidid>https://orcid.org/0000-0003-4710-0191</orcidid><oa>free_for_read</oa></addata></record> |
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identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2017-09, Vol.12 (9), p.e0184890-e0184890 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_1941341624 |
source | Open Access: PubMed Central; ProQuest - Publicly Available Content Database |
subjects | Abundance Age Animal health Animals Bacteria Biodiversity Biology and Life Sciences Bird Diseases - microbiology Bird Diseases - pathology Birds Broilers (Chickens) Causes of Cecum - microbiology Cecum - pathology Change detection Chickens Chickens - microbiology Coccidiosis Coccidiosis - microbiology Coccidiosis - pathology Coccidiosis - veterinary Development and progression Diseases and pests Drug resistance Dysbacteriosis E coli Eimeria tenella Enteritis Gastrointestinal Microbiome - genetics Genotype & phenotype Infections Inflammatory bowel disease Intervention Intestine Lesions Medicine and Health Sciences Microbiota (Symbiotic organisms) Microorganisms Parasites Pathology Phylogeny Physiological aspects Population Poultry Probiotics Random Allocation RNA, Ribosomal, 16S - genetics rRNA 16S Salmonella Sequence Analysis, DNA Severity of Illness Index Species diversity Taxa Veterinary colleges |
title | Effects of Eimeria tenella infection on chicken caecal microbiome diversity, exploring variation associated with severity of pathology |
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