Abstract
The buccal mucosa (BM) of vertebrates is a critical mucosal barrier constantly exposed to rich and diverse pathogens from air, water, and food. While mammals are known to contain a mucosal associated lymphoid tissue (MALT) in the buccal cavity which induces B-cells and immunoglobulins (Igs) responses against bacterial pathogens, however, very little is known about the evolutionary roles of buccal MALT in immune defense. Here we developed a bath infection model that rainbow trout experimentally exposed to Flavobacterium columnare (F. columnare), which is well known as a mucosal pathogen. Using this model, we provided the first evidence for the process of bacterial invasion in the fish BM. Moreover, strong pathogen-specific IgT responses and accumulation of IgT+ B-cells were induced in the buccal mucus and BM of infected trout with F. columnare. In contrast, specific IgM responses were for the most part detected in the fish serum. More specifically, we showed that the local proliferation of IgT+ B-cells and production of pathogen-specific IgT within the BM upon bacterial infection. Overall, our findings represent the first demonstration that IgT is the main Ig isotype specialized for buccal immune responses against bacterial infection in a non-tetrapod species.
Highlights
Due to its broad geographic distribution and ability to adhere to mucosal tissues, Flavobacterium columnare (F. columnare) is considered as one of the most harmful bacterial pathogens that occurs worldwide and causes columnaris disease in most freshwater fish species, including rainbow trout (Oncorhynchus mykiss) [1,2,3]
The tissue homogenates of trout buccal mucosa (BM) from control and 2-day-infected fish were both cultured on Shieh agar, and the bacterial colonies that were rhizoid and flat with yellow centers were detected only in infected trout. These single colonies were isolated to grow in pure culture, and characteristic elongated rod-shaped bacteria with green fluorescence were clearly observed by fluorescence microscope (Figure 1B), which further verified the successful invasion of F. columnare in trout BM after infection
While mammals’ buccal cavity (BC) is known to contain a mucosal associated lymphoid tissue (MALT), which plays a key role in the control of bacterial pathogens [10, 31], very little is known about the evolutionary origins of buccal MALT and its primordial roles in immune defense
Summary
Due to its broad geographic distribution and ability to adhere to mucosal tissues, Flavobacterium columnare (F. columnare) is considered as one of the most harmful bacterial pathogens that occurs worldwide and causes columnaris disease in most freshwater fish species, including rainbow trout (Oncorhynchus mykiss) [1,2,3]. Previous studies have showed that interaction with mucosal surfaces is critical for the pathogenesis and pathological symptoms of F. columnare [6, 7]. It’s necessary to understand the mechanisms responsible for mucosal immune responses to columnaris disease. The buccal cavity (BC) represents the gateway of the gastrointestinal (GI) and respiratory tracts in vertebrates [8], and it is covered by a critical mucosal barrier (buccal mucosa, BM) that separates and protects the underlying tissues from the environment [9].
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