Influenza A virus infection in turkeys induces respiratory and enteric bacterial dysbiosis correlating with cytokine gene expression

John M Ngunjiri; Kara J M Taylor; Hana Ji; Michael C Abundo; Amir Ghorbani; Mahesh Kc; Chang-Won Lee

doi:10.7717/peerj.11806

Influenza A virus infection in turkeys induces respiratory and enteric bacterial dysbiosis correlating with cytokine gene expression

PeerJ. 2021 Jul 22:9:e11806. doi: 10.7717/peerj.11806. eCollection 2021.

Authors

John M Ngunjiri^#¹, Kara J M Taylor^#^{1

2}, Hana Ji^{1

3}, Michael C Abundo¹, Amir Ghorbani^{1

3}, Mahesh Kc^{1

3

4}, Chang-Won Lee^{1

3}

Affiliations

¹ Center for Food Animal Health, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, OH, United States of America.
² Department of Biology, University of Florida, Gainesville, FL, United States of America.
³ Department of Veterinary Preventive Medicine, College of Veterinary Medicine, Ohio State University, Columbus, OH, United States of America.
⁴ Center for Vaccines and Immunity, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH, United States of America.

^# Contributed equally.

Abstract

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.

Keywords: Avian influenza virus; Dysbiosis; Proteobacteria; Respiratory microbiome; Virus-induced dysbiosis.

Grants and funding

This project was supported by Agriculture and Food Research Initiative competitive grant number (2015-68004-23131) from the USDA National Institute of Food and Agriculture (to Chang-Won Lee). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.