Rainbow trout (Oncorhynchus mykiss) secretory component binds to commensal bacteria and pathogens

Cecelia Kelly,Irene Salinas,J Oriol Sunyer,Fumio Takizawa

doi:10.1038/srep41753

Cecelia Kelly, Irene Salinas + Show 2 more

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https://doi.org/10.1038/srep41753

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Abstract

Commensal bacteria co-exist on the mucosal surfaces of all vertebrates. The host’s mucosal immune system must tolerate commensals while fighting pathogens. One of the mechanisms used by the mucosal immune system to maintain homeostasis is the secretion of immunoglobulins (Igs) across epithelial barriers, which is achieved via the polymeric immunoglobulin receptor (pIgR). Rainbow trout pIgR is known to transport IgT and IgM across epithelia. However, other biological functions for trout pIgR or trout secretory component (tSC) remain unknown. This study investigates the interaction of tSC with commensal bacteria, pathogenic bacteria and a fungal pathogen. Our results show that the majority of trout skin and gut bacteria are coated in vivo by tSC. In vitro, tSC present in mucus coats trout commensal isolates such as Microbacterium sp., Staphylococcus warneri, Flectobacillus major, Arthrobacter stackebrantii, and Flavobacterium sp. and the pathogens Vibrio anguillarum and Edwardsiella ictaluri with coating levels ranging from 8% to 70%. Moreover, we found that the majority of tSC is in free form in trout mucus and free tSC is able to directly bind bacteria. We propose that binding of free SC to commensal bacteria is a key and conserved mechanism for maintenance of microbial communities in vertebrate mucosal surfaces.

Highlights

Commensal bacteria co-exist on the mucosal surfaces of all vertebrates
In order to show that rainbow trout gut and skin commensals are coated in vivo with polymeric immunoglobulin receptor (pIgR)/secretory component (SC), we examined freshly isolated trout skin and gut bacteria using immunofluorescence microscopy
We observed that 64% of bacteria isolated from the skin were coated with pIgR, while 79% of gut bacteria were coated with pIgR, compared to background coating levels with the prebleed antibody of 20% and 9% in skin and gut, respectively (Fig. 1a–c)

Summary

Introduction

Commensal bacteria co-exist on the mucosal surfaces of all vertebrates. The host’s mucosal immune system must tolerate commensals while fighting pathogens. Our results show that the majority of trout skin and gut bacteria are coated in vivo by tSC. We propose that binding of free SC to commensal bacteria is a key and conserved mechanism for maintenance of microbial communities in vertebrate mucosal surfaces. The cysteine required for this disulphide bond is absent in D55, and there is no known J-chain present in trout sIgs for D1 to associate with[8,9]. The sIg-SC complex is known to limit access of microbes to the epithelium and help to control commensal populations. This is achieved through antigen specific, Fab-mediated binding and innate Fab-independent (glycan mediated) binding, both present in www.nature.com/scientificreports/.

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