The bursa of Fabricius is a primary and secondary lymphoid organ considered exclusively present in birds, and studies of this structure have been vital to our current understanding of the adaptive immune system of vertebrates. In this study, we reveal substantial lymphoepithelial tissue in a previously undescribed bursa in Atlantic salmon (Salmo salar), situated caudal to the urogenital papilla of the cloaca and thus analogous to the anatomical placement of the bursa of Fabricius. We investigated three groups of Atlantic salmon at different maturational stages and characterized the structure by applying dissection, radiology, scanning electron microscopy and histological techniques, including immunohistochemistry and in situ hybridization. We found that the epithelial anlage of the salmon cloacal bursa developed into substantial lymphoepithelial tissue and subsequently regressed following sexual maturation. Such a dynamic development is also a key characteristic of the avian bursa. The presence of intraepithelial lymphocytes was concomitant with expression of the leukocyteattracting chemokine CCL19, indicative of lymphoid organ functions. We did not observe recombination or gene conversion in salmon bursal lymphocytes at any developmental stage, indicating the absence of primary lymphoid organ functions in contrast to the bursa of Fabricius. However, the possibility of the bursa to trap both enteric and environmental antigens, combined with the presence of several antigen-presenting cells residing within the lymphoepithelium, suggest the structure has secondary lymphoid organ functions. We present the discovery of a lymphoid organ in Atlantic salmon with striking topographical similarities to that of the bursa of Fabricius in birds. In addition, the age-dependent dynamics of its lymphoepithelium suggest functions related to the maturation processes of lymphocytes.

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Knowledge of the construction of immune organs of different species is important to understand the evolution of immunity. In birds, the bursa of Fabricius is a cloaca-based lymphoid organ that has been vital for our current understanding of the adaptive immune system of vertebrates. So far, this structure has not been described in other species. Here, we show a substantial lymphoepithelial tissue in a previously undescribed bursa in the Atlantic salmon, situated analogous to the placement of the avian bursa of Fabricius, also developing from the ectoderm. Investigations of three different age groups of Atlantic salmon revealed a dynamic lymphoepithelium that regressed following sexual maturation. This is similar to the situation in birds. Morphological investigations including dissection, radiography, in situ hybridization and immunohistochemistry revealed presence of T and B cells embedded within a CCL19-positive lymphoepithelium. CCL19 expression is indicative for lymphoid organs, and thus we suggest that the salmonid bursa should be regarded as such. We found however no evidence for primary lymphoid organ functions including recombination events in the lymphocytes, this contrasting the situation in birds. Our results demonstrate the presence of a salmonid lymphoepithelial compartment with anatomical and developmental similarities to early stages in the organogenesis of the avian bursa of Fabricius. Such information provides novel and exciting possibilities both for our understanding of the function of the immune system in salmon and for our understanding of the development of lymphoid structures and niches in vertebrates.

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