Gas exchange structures are critical for acquiring oxygen, but hey also represent portals for pathogen entry. Local mucosal immunoglobulin (Ig) responses against pathogens in specialized respiratory organshave only been described in tetrapods. We have previously shown that IgT is an Ig specialized in gut andskin mucosal immunity. Thus, we tested the hypothesis that IgT might play a pivotal role in mucosalimmunity of teleost gills. In this study, we provide the first structural and functional characterization of allteleost Igs, including secreted IgD, IgM and IgT at a mucosal surface of a teleost fish. Here we show thatIgT+ B cells represent the major B cell subset in the gill filaments. In contrast to reported results by others,we found that all gill B cells expressing surface IgM, also expressed surface IgD and that the percentageof B cells solely expressing either IgD or IgM was negligible. We found that the majority of bacterialmicrobiota in the gill mucosa is coated with IgT and, to a much lesser degree with IgM and IgD. Morecrucially, significant specific-IgT immune responses against Ichthyophthirius multifiliis (Ich) andFlavobacterium columnare were measured in the gill mucus, while pathogen-specific IgM responses werealmost exclusively detected in the serum. Pathogen-specific IgD titers were absent both in gill mucus andserum. Importantly, we found significant IgT+ B-cell proliferative responses in the gill but not in thespleen or head kidney of fish that survived Ich infection. Moreover we also found that Ich- and F.columnare-specific IgT titers were locally produced by gill explants of survivor fish while they wereabsent in the spleen or head kidney explants of the same animals. In addition to showing that IgT is themain Ig player in gill mucosal immunity, the observed generation of local IgT+ B cell proliferative andpathogen-specific IgT responses in the gills provides the first demonstration of locally induced B cell andsecretory Ig responses in the mucosa of a teleost. Moreover, this represents the first study in which abacterial pathogen is shown to induce dominant IgT responses in a fish mucosal site, thus stronglysuggesting that IgT is induced by a variety of pathogens in addition to parasites. Our findings also havespecial relevance from an applied perspective as they may lead to the development of fish vaccines andimmunostimulants that have the capacity to induce gill IgT mucosal immune responses.