Abstract
SummaryThe 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.
Highlights
The buccal cavity (BC) of vertebrates is the gateway for both the gastrointestinal and respiratory tracts and is considered a critical mucosal surface in tetrapod species (Winning and Townsend, 2000; Squier and Kremer, 2001; Abbate et al, 2006)
Teleost buccal mucosa (BM) Shares the Typical Features of a mucosal associated lymphoid tissue (MALT) To understand the histological organization of teleost BM (Figures S1A–S1D), paraffin sections of BMs obtained from five different families (Figure S2), Salmonidae, Percichthyidae, Synbranchidae, Siluridae, and Channidae, were stained with both hematoxylin and eosin (H&E) (Figures 1A–1E) and Alcian blue (AB) (Figures 1F and S3A–S3D)
We observed that the BM of Japanese sea bass (Lateolabrax japonicus), Asian swamp eel (Monopterus albus), Southern catfish (Silurus meridionalis), and Snakehead (Channa argus) contained intraepithelial lymphocytes and lamina propria leukocytes (Figures 1A–1E), with a large number of mucus-producing cells in the buccal epithelium (Figures 1F and S3A–S3D)
Summary
The buccal cavity (BC) of vertebrates is the gateway for both the gastrointestinal and respiratory tracts and is considered a critical mucosal surface in tetrapod species (Winning and Townsend, 2000; Squier and Kremer, 2001; Abbate et al, 2006). Secretory IgA (sIgA) is the main humoral component involved in adaptive immune responses against oral pathogens (Brandtzaeg, 2013). Amphibians are known to contain both mucus-producing cells as well as intermaxillary salivary glands (Latney and Clayton, 2014), the digestive and adaptive immune roles of their putative saliva and mucosal secretions have been ill investigated. In contrast to all tetrapod species, teleost fish lack salivary glands in their BC, which is instead populated with abundant mucus-secreting cells that produce the mucus that coats their buccal epithelium (Yashpal et al, 2007)
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