Lymphoid Tissue in Teleost Gills: Variations on a Theme

Abstract

In bony fish, the gill filaments are essential for gas exchanges, but also are vulnerable to infection by water-borne microorganisms. Omnipresent across fish, gill-associated lymphoid tissues (GIALT) regulate interactions with local microbiota and halt infection by pathogens. A special GIALT structure has recently been found in Salmonids, the interbranchial lymphoid tissue (ILT). However, the structural variation of GIALT across bony fish remains largely unknown. Here, we show how this critical zone of interaction evolved across fishes. By labeling a conserved T-cell epitope on tissue sections, we find that several basal groups of teleosts possess typical ILT, while modern teleosts have lymphoepithelium of different shape and size at the base of primary gill filaments. Within Cypriniformes, neither body size variation between two related species, zebrafish and common carp, nor morphotype variation, did have a drastic effect on the structure of ILT. Thereby this study is the first to describe the presence of ILT in zebrafish. The ILT variability across fish orders seems to represent different evolutionary solutions to balancing trade-offs between multiple adaptations of jaws and pharyngeal region, and immune responses. Our data point to a wide structural variation in gill immunity between basal groups and modern teleosts.

High-Resolution, 3D Imaging of the Zebrafish Gill-Associated Lymphoid Tissue (GIALT) Reveals a Novel Lymphoid Structure, the Amphibranchial Lymphoid Tissue

“…However, the absence of O-MALT structures in teleosts has been challenged by the identification of a lymphoid tissue structured by reticulated epithelial cells in the gills of Atlantic salmon ( Salmo salar L. ), called the “Interbranchial lymphoid tissue” (ILT) ( 42 , 43 ). This structure proved also to be present in a number of other teleost species, including the zebrafish ( 44 ). This finding underlines the need to improve our knowledge of the lymphoid organization of zebrafish gills.…”

“…The anti-inflammatory cytokine IL-10 seems to be an important factor for gill homeostasis in zebrafish ( 56 ). Zebrafish gill’s defenses consist of many scattered myeloid cells, lymphoid cells, and myeloid-like metaphocytes ( 16 , 21 , 44 , 57 ). The sampling of foreign antigens is performed by both epithelial cells and immune cells from the gill mucosa.…”

Anatomy of teleost fish immune structures and organs

“…5 ) was first discovered and described about 10 years ago (Haugarvoll et al 2008 ). It has later become apparent that such lymphoid aggregates not only are present in salmonids but may also be found in several other teleost species (Rességuier et al 2020 ). The ILT is situated between the primary lamellae at the distal extension of the intralamellar septum and was thus named the “interbranchial lymphoid tissue” or “ILT” by Koppang et al ( 2010 ).…”

Immunologic Profiling of the Atlantic Salmon Gill by Single Nuclei Transcriptomics

“…The salmonid gill is a complex multifunctional organ, essential for gas exchange, nitrogenous waste excretion, pH balance and osmoregulation ( 3 ). It is also a major mucosal immune barrier harboring a dedicated lymphoid tissue termed gill associated lymphoid tissue (GIALT) ( 4 , 5 ) which is rich in T cells, natural killer cells and macrophages. Although it is known that smoltification suppresses immune function, little, if anything, is known about which immune cell types in the gill are modified ( 6 ).…”