Convergent Evolution of Mucosal Immune Responses at the Buccal Cavity of Teleost Fish

The buccal mucosa (BM) is a critical first line of defense in terrestrial animals. To gain further insights into the evolutionary origins and primordial roles of BM in teleosts here we show that rainbow trout, a teleost fish, contains a diffuse mucosal associated lymphoid tissue (MALT) within its bu...

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Published iniScience Vol. 19; pp. 821 - 835
Main Authors Yu, Yong-Yao, Kong, Wei-Guang, Xu, Hao-Yue, Huang, Zhen-Yu, Zhang, Xiao-Ting, Ding, Li-Guo, Dong, Shuai, Yin, Guang-Mei, Dong, Fen, Yu, Wei, Cao, Jia-Feng, Meng, Kai-Feng, Liu, Xia, Fu, Yu, Zhang, Xue-zhen, Zhang, Yong-an, Sunyer, J. Oriol, Xu, Zhen
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 27.09.2019
Elsevier
Subjects
Biological Sciences
convergent evolution
Immunology
mammals
microorganisms
mouth
mucosa
mucosal immunity
mucus
Omics
Oncorhynchus mykiss
parasites
Transcriptomics
trout
Biological Sciences
Immunology
Transcriptomics
Omics
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Summary:The buccal mucosa (BM) is a critical first line of defense in terrestrial animals. To gain further insights into the evolutionary origins and primordial roles of BM in teleosts here we show that rainbow trout, a teleost fish, contains a diffuse mucosal associated lymphoid tissue (MALT) within its buccal cavity. Upon parasite infection, a fish immunoglobulin specialized in mucosal immunity (sIgT) was induced to a high degree, and parasite-specific sIgT responses were mainly detected in the buccal mucus. Moreover, we show that the trout buccal microbiota is prevalently coated with sIgT. Overall our findings revealed that the MALT is present in the BM of a non-tetrapod species. As fish IgT and mucus-producing cells are evolutionarily unrelated to mammalian IgA and salivary glands, respectively, our findings indicate that mucosal immune responses in the BM of teleost fish and tetrapods evolved through a process of convergent evolution. [Display omitted] •A mucosal associated lymphoid tissue is identified in teleost buccal cavity•Local immune responses can be induced in teleost buccal mucosa•Teleost IgT plays important roles in defending against buccal pathogen•Microbiota in teleost buccal mucosa is prevalently coated with secreted IgT Biological Sciences; Immunology; Omics; Transcriptomics
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These authors contributed equally
ISSN:2589-0042
2589-0042
DOI:10.1016/j.isci.2019.08.034