Symbiont-derived sphingolipids modulate mucosal homeostasis and B cells in teleost fish.

Ali Sepahi,Héctor Cordero,Maria Ángeles Esteban,Irene Salinas,Howard Goldfine

doi:10.1038/srep39054

Ali Sepahi, Héctor Cordero + Show 3 more

Open Access

https://doi.org/10.1038/srep39054

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Abstract

Symbiotic bacteria and mucosal immunoglobulins have co-evolved for millions of years in vertebrate animals. Symbiotic bacteria products are known to modulate different aspects of the host immune system. We recently reported that Flectobacillus major is a predominant species that lives in the gill and skin mucosal surfaces of rainbow trout (Oncorhynchus mykiss). F. major is known to produce sphingolipids of a unique molecular structure. Here we propose a role for F. major and its sphingolipids in the regulation of B cell populations in rainbow trout, as well as an essential role for sphingolipids in trout mucosal homeostasis. We found that F. major-specific IgT titers are confined to the gill and skin mucus, whereas F. major-specific IgM titers are only detected in serum. Live F. major cells are able to stimulate sustained IgT expression and secretion in gills. F. major sphingolipids modulate the growth of trout total skin and gill symbiotic bacteria. In vivo systemic administration of F. major sphingolipids changes the proportion of IgT+ to IgM+ B cells in trout HK. These results demonstrate the key role of the symbiont F. major and its sphingolipids in mucosal homeostasis via the modulation of mucosal and systemic Igs and B cells.

Highlights

Symbiotic bacteria and mucosal immunoglobulins have co-evolved for millions of years in vertebrate animals
Upon symbiont removal, specific IgT could no longer be detected in skin mucus samples indicating that all the F. major-specific IgT in skin mucus was bound to bacteria present in the samples
Removal of bacteria from gill mucus did not eliminate the presence of specific IgT in the sample, indicating that F. major-specific IgT antibodies are present in free form in trout gill mucus (Table 1, Fig. 1)

Summary

Introduction

Symbiotic bacteria and mucosal immunoglobulins have co-evolved for millions of years in vertebrate animals. The animal host needs to tolerate symbionts while fighting pathogens, a complex process for the animal’s immune system[1,7,8] Teleost fish such as rainbow trout (Oncorhynchus mykiss) have numerous mucosal barriers such as the gut, skin, gills and olfactory organ that separate them from the environment. F. major had not been reported to be a member of the microbiome of any fish species, likely due to the lack of pyrosequencing studies from these two sites This strong association, suggested that F. major may play a major role in the gill and skin mucosal immune system of rainbow trout

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