Research progress and prospect in mucosal B cells and immunoglobulins of teleost fish

Abstract

<p indent="0mm">Fish live in a microbially rich and complex aquatic environment, which exposes their mucosal surfaces to a variety of attacks from external pathogens. Teleost fish have evolved unique mucosa-associated lymphoid tissues (MALTs) that serve as the first line of defense against pathogens. So far, seven MALTs in teleost fish have been described, including gut-associated lymphoid tissue (GALT), skin-associated lymphoid tissue (SALT), gill-associated lymphoid tissue (GIALT), nasal-associated lymphoid tissue (NALT), buccal-associated lymphoid tissues, pharyngeal-associated lymphoid tissues, and the newly discovered swim bladder-associated lymphoid tissues. Because teleost MALT lacks lymph nodes, it has only evolved as a network of diffuse leucocytes within the mucosal epithelia, which is known as diffuse MALT (D-MALT). Teleost fish, unlike invertebrates, have evolved the cardinal elements of adaptive immunity to protect themselves from pathogens in their aquatic environment. Mucosal B cells and immunoglobulins (Igs) in teleost MALTs, in particular, are important players in local mucosal adaptive immune responses. In teleost fish, the three bona fide immunoglobulin isotypes (i.e., IgM, IgD, and IgT) can be found in varying proportions in MALT secretions, and the IgT/IgM ratio in mucus is much higher than that in serum in the absence of antigenic stimulation. A couple of functional studies have recently revealed that IgM and IgT responses are specialized in systemic and mucosal compartments, respectively. The primary role of Igs in adaptive immune responses has been conserved throughout evolution, as they can neutralize pathogens or promote their elimination on mucosal surfaces, preventing further infection. Teleost fish lack organized lymphoid structures known as O-MALT (e.g., Peyer’s patches and tonsils), but B-cells could locally proliferate and generate pathogenic-specific Igs in the MALTs, indicating that MALT in teleosts may function as both an inductive and effector site. Mucosal surfaces in teleost MALT harbor an incredibly dense and diverse commensal microbiota, which is one of the conserved features. Notably, a significant portion of the commensal microbiota is coated with secreted Igs (sIgs), with IgT being the predominant isotype associated with those bacteria. Recent advances in bacterial flow cytometry combined with high-throughput sequencing have aided in the identification of IgT-coated bacteria and shed light on the biological implications of sIgs coating commensal microbiota. Teleost fish secretory IgT, like mammalian and bird IgA, may target mucosal pathogens for elimination, and coating on the surface of microbiota allows for commensal colonization and homeostasis. Therefore, studying and revealing the immunological mechanism of fish MALT in anti-infection and maintaining mucosal commensal homeostasis is extremely important in fish immunology and even vertebrate comparative immunology in general. We summarize the current research process on the composition of the fish mucosal immune system, the function of mucosal B cells and Igs against pathogen infections, and the interactions between sIgs and microbiota in this review. Finally, we outline the future prospects for fish mucosal immunity, with the goal of providing a reference from a mucosal vaccination standpoint for the prevention and control of fish diseases.