Heritable Gut Microbiome Associated with <italic toggle="yes">Salmonella enterica</italic> Serovar Pullorum Infection in Chickens

Jinmei Ding; Hao Zhou; Lingxiao Luo; Lu Xiao; Kaixuan Yang; Lingyu Yang; Yuming Zheng; Ke Xu; Chuan He; Chengxiao Han; Huaixi Luo; Chao Qin; Fisayo T. Akinyemi; Caiju Gu; Zhenxiang Zhou; Qizhong Huang; He Meng

doi:10.1128/mSystems.01192-20

mSystems (Feb 2021)

Heritable Gut Microbiome Associated with <italic toggle="yes">Salmonella enterica</italic> Serovar Pullorum Infection in Chickens

Jinmei Ding,
Hao Zhou,
Lingxiao Luo,
Lu Xiao,
Kaixuan Yang,
Lingyu Yang,
Yuming Zheng,
Ke Xu,
Chuan He,
Chengxiao Han,
Huaixi Luo,
Chao Qin,
Fisayo T. Akinyemi,
Caiju Gu,
Zhenxiang Zhou,
Qizhong Huang,
He Meng

Affiliations

Jinmei Ding: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China
Hao Zhou: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China
Lingxiao Luo: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China
Lu Xiao: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China
Kaixuan Yang: Animal Husbandry and Veterinary Research Institute, Shanghai Academy of Agricultural Science, Shanghai, People’s Republic of China
Lingyu Yang: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China
Yuming Zheng: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China
Ke Xu: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China
Chuan He: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China
Chengxiao Han: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China
Huaixi Luo: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China
Chao Qin: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China
Fisayo T. Akinyemi: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China
Caiju Gu: Animal Husbandry and Veterinary Research Institute, Shanghai Academy of Agricultural Science, Shanghai, People’s Republic of China
Zhenxiang Zhou: Animal Husbandry and Veterinary Research Institute, Shanghai Academy of Agricultural Science, Shanghai, People’s Republic of China
Qizhong Huang: Animal Husbandry and Veterinary Research Institute, Shanghai Academy of Agricultural Science, Shanghai, People’s Republic of China
He Meng: Shanghai Key Laboratory of Veterinary Biotechnology, Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, People’s Republic of China

DOI: https://doi.org/10.1128/mSystems.01192-20
Journal volume & issue: Vol. 6, no. 1

Abstract

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ABSTRACT Pullorum disease is one of the most common diarrhea-related diseases caused by Salmonella enterica subspecies enterica serovar Gallinarum biovar Pullorum (S. Pullorum); it negatively affects the poultry industry. However, limited studies have explored the association between the gut microbiota and S. Pullorum infection in chickens. In the present study, we performed a microbiome comparison and a microbiome genome-wide association study (mGWAS) to investigate the association among the host genetics, the gut microbiota, and pullorum disease in chickens. We found that S. Pullorum infection in chickens could alter the abundance of 39 bacterial genera (P < 0.05). The altered structure and composition of the gut microbiota were also detected in the offspring. mGWAS results revealed host genetic variants to be prominently associated with gut microbial diversity and individual microbes. The pathogens Pelomonas and Brevundimonas, which had a high abundance in positive parent chickens and their offspring, were significantly associated with several genetic mutations in immunity-related genes, such as TGIF1, TTLL12, and CCR7. This finding explained why Pelomonas and Brevundimonas were heritable in S. Pullorum-infected chickens. The heritable gut microbes and identified genetic variants could provide references for the selection of resistant chickens and the elimination of pullorum disease. IMPORTANCE The present study investigated the association among the host genome, the gut microbiome, and S. Pullorum infection in chickens. The results suggested that the gut microbial structure is altered in S. Pullorum-infected chickens. The diversity and abundance of the gut microbiota remarkably differed between the offspring coming from S. Pullorum-positive and S. Pullorum-negative chickens. Heritable gut microbiota were detected in the offspring. Moreover, host genetic variants were associated with microbial diversity and individual gut microbes. The pathogens Pelomonas and Brevundimonas, which exhibited a high heritability in S. Pullorum-positive parents and their offspring, were associated with several genetic mutations in immunity-related genes.

Published in mSystems

ISSN: 2379-5077 (Online)
Publisher: American Society for Microbiology
Country of publisher: United States
LCC subjects: Science: Microbiology
Website: https://journals.asm.org/journal/msystems

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