Influenza A virus infection in turkeys induces respiratory and enteric bacterial dysbiosis correlating with cytokine gene expression
Turkey respiratory and gut microbiota play important roles in promoting health and production performance. Loss of microbiota homeostasis due to pathogen infection can worsen the disease or predispose the bird to infection by other pathogens. While turkeys are highly susceptible to influenza viruses...
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| Format: | Article |
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PeerJ Inc.
2021-07-01
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| Online Access: | https://peerj.com/articles/11806.pdf |
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| author | John M. Ngunjiri Kara J.M. Taylor Hana Ji Michael C. Abundo Amir Ghorbani Mahesh KC Chang-Won Lee |
| author_facet | John M. Ngunjiri Kara J.M. Taylor Hana Ji Michael C. Abundo Amir Ghorbani Mahesh KC Chang-Won Lee |
| author_sort | John M. Ngunjiri |
| collection | DOAJ |
| description | Turkey respiratory and gut microbiota play important roles in promoting health and production performance. Loss of microbiota homeostasis due to pathogen infection can worsen the disease or predispose the bird to infection by other pathogens. While turkeys are highly susceptible to influenza viruses of different origins, the impact of influenza virus infection on turkey gut and respiratory microbiota has not been demonstrated. In this study, we investigated the relationships between low pathogenicity avian influenza (LPAI) virus replication, cytokine gene expression, and respiratory and gut microbiota disruption in specific-pathogen-free turkeys. Differential replication of two LPAI H5N2 viruses paralleled the levels of clinical signs and cytokine gene expression. During active virus shedding, there was significant increase of ileal and nasal bacterial contents, which inversely corresponded with bacterial species diversity. Spearman’s correlation tests between bacterial abundance and local viral titers revealed that LPAI virus-induced dysbiosis was strongest in the nasal cavity followed by trachea, and weakest in the gut. Significant correlations were also observed between cytokine gene expression levels and relative abundances of several bacteria in tracheas of infected turkeys. For example, interferon γ/λ and interleukin-6 gene expression levels were correlated positively with Staphylococcus and Pseudomonas abundances, and negatively with Lactobacillus abundance. Overall, our data suggest a potential relationship where bacterial community diversity and enrichment or depletion of several bacterial genera in the gut and respiratory tract are dependent on the level of LPAI virus replication. Further work is needed to establish whether respiratory and enteric dysbiosis in LPAI virus-infected turkeys is a result of host immunological responses or other causes such as changes in nutritional uptake. |
| first_indexed | 2024-03-09T08:08:43Z |
| format | Article |
| id | doaj.art-86723a96cfa34c9093d58aca9d8dab5e |
| institution | Directory Open Access Journal |
| issn | 2167-8359 |
| language | English |
| last_indexed | 2024-03-09T08:08:43Z |
| publishDate | 2021-07-01 |
| publisher | PeerJ Inc. |
| record_format | Article |
| series | PeerJ |
| spelling | doaj.art-86723a96cfa34c9093d58aca9d8dab5e2023-12-02T23:33:35ZengPeerJ Inc.PeerJ2167-83592021-07-019e1180610.7717/peerj.11806Influenza A virus infection in turkeys induces respiratory and enteric bacterial dysbiosis correlating with cytokine gene expressionJohn M. Ngunjiri0Kara J.M. Taylor1Hana Ji2Michael C. Abundo3Amir Ghorbani4Mahesh KC5Chang-Won Lee6Center for Food Animal Health, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, OH, United States of AmericaCenter for Food Animal Health, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, OH, United States of AmericaCenter for Food Animal Health, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, OH, United States of AmericaCenter for Food Animal Health, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, OH, United States of AmericaCenter for Food Animal Health, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, OH, United States of AmericaCenter for Food Animal Health, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, OH, United States of AmericaCenter for Food Animal Health, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, OH, United States of AmericaTurkey respiratory and gut microbiota play important roles in promoting health and production performance. Loss of microbiota homeostasis due to pathogen infection can worsen the disease or predispose the bird to infection by other pathogens. While turkeys are highly susceptible to influenza viruses of different origins, the impact of influenza virus infection on turkey gut and respiratory microbiota has not been demonstrated. In this study, we investigated the relationships between low pathogenicity avian influenza (LPAI) virus replication, cytokine gene expression, and respiratory and gut microbiota disruption in specific-pathogen-free turkeys. Differential replication of two LPAI H5N2 viruses paralleled the levels of clinical signs and cytokine gene expression. During active virus shedding, there was significant increase of ileal and nasal bacterial contents, which inversely corresponded with bacterial species diversity. Spearman’s correlation tests between bacterial abundance and local viral titers revealed that LPAI virus-induced dysbiosis was strongest in the nasal cavity followed by trachea, and weakest in the gut. Significant correlations were also observed between cytokine gene expression levels and relative abundances of several bacteria in tracheas of infected turkeys. For example, interferon γ/λ and interleukin-6 gene expression levels were correlated positively with Staphylococcus and Pseudomonas abundances, and negatively with Lactobacillus abundance. Overall, our data suggest a potential relationship where bacterial community diversity and enrichment or depletion of several bacterial genera in the gut and respiratory tract are dependent on the level of LPAI virus replication. Further work is needed to establish whether respiratory and enteric dysbiosis in LPAI virus-infected turkeys is a result of host immunological responses or other causes such as changes in nutritional uptake.https://peerj.com/articles/11806.pdfRespiratory microbiomeDysbiosisProteobacteriaAvian influenza virusVirus-induced dysbiosis |
| spellingShingle | John M. Ngunjiri Kara J.M. Taylor Hana Ji Michael C. Abundo Amir Ghorbani Mahesh KC Chang-Won Lee Influenza A virus infection in turkeys induces respiratory and enteric bacterial dysbiosis correlating with cytokine gene expression PeerJ Respiratory microbiome Dysbiosis Proteobacteria Avian influenza virus Virus-induced dysbiosis |
| title | Influenza A virus infection in turkeys induces respiratory and enteric bacterial dysbiosis correlating with cytokine gene expression |
| title_full | Influenza A virus infection in turkeys induces respiratory and enteric bacterial dysbiosis correlating with cytokine gene expression |
| title_fullStr | Influenza A virus infection in turkeys induces respiratory and enteric bacterial dysbiosis correlating with cytokine gene expression |
| title_full_unstemmed | Influenza A virus infection in turkeys induces respiratory and enteric bacterial dysbiosis correlating with cytokine gene expression |
| title_short | Influenza A virus infection in turkeys induces respiratory and enteric bacterial dysbiosis correlating with cytokine gene expression |
| title_sort | influenza a virus infection in turkeys induces respiratory and enteric bacterial dysbiosis correlating with cytokine gene expression |
| topic | Respiratory microbiome Dysbiosis Proteobacteria Avian influenza virus Virus-induced dysbiosis |
| url | https://peerj.com/articles/11806.pdf |
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