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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Abstract 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
AbstractList 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. : Biological Sciences; Immunology; Omics; Transcriptomics Subject Areas: Biological Sciences, Immunology, Omics, Transcriptomics
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. • 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
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
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.
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.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.
Author Zhang, Yong-an
Huang, Zhen-Yu
Yu, Wei
Fu, Yu
Zhang, Xue-zhen
Dong, Fen
Xu, Zhen
Kong, Wei-Guang
Xu, Hao-Yue
Liu, Xia
Cao, Jia-Feng
Yu, Yong-Yao
Sunyer, J. Oriol
Dong, Shuai
Zhang, Xiao-Ting
Meng, Kai-Feng
Ding, Li-Guo
Yin, Guang-Mei
AuthorAffiliation 3 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, Shandong 266071, China
1 Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
2 Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
AuthorAffiliation_xml – name: 2 Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
– name: 1 Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
– name: 3 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, Shandong 266071, China
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  givenname: Wei-Guang
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  organization: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
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  givenname: Li-Guo
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  organization: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
– sequence: 7
  givenname: Shuai
  surname: Dong
  fullname: Dong, Shuai
  organization: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
– sequence: 8
  givenname: Guang-Mei
  surname: Yin
  fullname: Yin, Guang-Mei
  organization: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
– sequence: 9
  givenname: Fen
  surname: Dong
  fullname: Dong, Fen
  organization: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
– sequence: 10
  givenname: Wei
  surname: Yu
  fullname: Yu, Wei
  organization: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
– sequence: 11
  givenname: Jia-Feng
  surname: Cao
  fullname: Cao, Jia-Feng
  organization: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
– sequence: 12
  givenname: Kai-Feng
  surname: Meng
  fullname: Meng, Kai-Feng
  organization: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
– sequence: 13
  givenname: Xia
  surname: Liu
  fullname: Liu, Xia
  organization: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
– sequence: 14
  givenname: Yu
  surname: Fu
  fullname: Fu, Yu
  organization: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
– sequence: 15
  givenname: Xue-zhen
  surname: Zhang
  fullname: Zhang, Xue-zhen
  organization: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
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  givenname: Yong-an
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  email: zhenxu@mail.hzau.edu.cn
  organization: Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31499339$$D View this record in MEDLINE/PubMed
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Keywords Biological Sciences
Immunology
Transcriptomics
Omics
Language English
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Snippet 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...
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SubjectTerms Biological Sciences
convergent evolution
Immunology
mammals
microorganisms
mouth
mucosa
mucosal immunity
mucus
Omics
Oncorhynchus mykiss
parasites
Transcriptomics
trout
Title Convergent Evolution of Mucosal Immune Responses at the Buccal Cavity of Teleost Fish
URI https://dx.doi.org/10.1016/j.isci.2019.08.034
https://www.ncbi.nlm.nih.gov/pubmed/31499339
https://www.proquest.com/docview/2288010281
https://www.proquest.com/docview/2660983794
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