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.

Highlights

  • The pharyngeal pouches and slits are a fundamental structure shared by all deuterostomes

  • The first report of a defined structure in the gill-associated lymphoid tissue (GIALT) of a teleost fish was the discovery of the interbranchial lymphoid tissue (ILT) in the gills of Atlantic salmon (Figure 3A)

  • A monoclonal against the highly conserved Syk family protein tyrosine kinase Zap-70 that is expressed by T cells and NK cells, and known to play a critical role in mediating T-cell activation that is expressed by T cells and NK cells, and known to play a critical role in mediating T-cell in response to T-cell receptor (TCR) engagement

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Summary

Introduction

The pharyngeal pouches and slits are a fundamental structure shared by all deuterostomes. Gills are present within pharyngeal pouches of all vertebrates during embryogenesis, but they fully develop in adult forms of aquatic fishes. This paraphyletic group comprises lampreys and hagfish (Agnathans), cartilaginous fishes (Chondrichthyes) including sharks and rays with a skeleton made of cartilage, and bony fishes (Osteichthyes) with a skeleton made of bone, including the modern bony fishes (Teleostei), [1]. With a vast and complex folded surface, gills are considered crucial for O2 uptake, energy turnover and exchange of ions and CO2. Biology 2020, 9, 127; doi:10.3390/biology9060127 www.mdpi.com/journal/biology exchange of ions and CO2

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