Gut immunity in a protochordate involves a secreted immunoglobulin-type mediator binding host chitin and bacteria.

Larry J Dishaw,John P Cannon,Gary W Litman,Brittany Leigh,Maria R Pinto,Diana P Skapura,Assunta Liberti,Rosaria De Santis,Charlotte R Karrer,M Gail Mueller

doi:10.1038/ncomms10617

Abstract

Protochordate variable region-containing chitin-binding proteins (VCBPs) consist of immunoglobulin-type V domains and a chitin-binding domain (CBD). VCBP V domains facilitate phagocytosis of bacteria by granulocytic amoebocytes; the function of the CBD is not understood. Here we show that the gut mucosa of Ciona intestinalis contains an extensive matrix of chitin fibrils to which VCBPs bind early in gut development, before feeding. Later in development, VCBPs and bacteria colocalize to chitin-rich mucus along the intestinal wall. VCBP-C influences biofilm formation in vitro and, collectively, the findings of this study suggest that VCBP-C may influence the overall settlement and colonization of bacteria in the Ciona gut. Basic relationships between soluble immunoglobulin-type molecules, endogenous chitin and bacteria arose early in chordate evolution and are integral to the overall function of the gut barrier.

Highlights

Protochordate variable region-containing chitin-binding proteins (VCBPs) consist of immunoglobulin-type V domains and a chitin-binding domain (CBD)
In chordate taxa that diverged before the evolutionary emergence of adaptive immunity, soluble immune mediators encoding V-type immunoglobulin domains likely serve a role in the establishment and maintenance of gut homeostasis by modulating bacterial community structure
Thick ribbon-like chitin-rich mucus often is seen accumulating at the base of the stomach epithelial folds (Supplementary Fig. 1b), consistent with the stomach epithelial expression patterns of VCBP-C (Supplementary Fig. 1c)[6]

Summary

Introduction

Protochordate variable region-containing chitin-binding proteins (VCBPs) consist of immunoglobulin-type V domains and a chitin-binding domain (CBD). We show that the gut mucosa of Ciona intestinalis contains an extensive matrix of chitin fibrils to which VCBPs bind early in gut development, before feeding. Protochordate species lack an adaptive immune system but possess multigene families of innate immune receptors[1], including the secreted immunoglobulin variable region-containing chitin-binding proteins (VCBPs)[2], which are not found in vertebrates. The V-region domains[4] of VCBPs bind and promote the opsonization of bacteria[5]; the distinctive C-terminal chitin-binding domain (CBD) likely is integral to overall function[2,5,6]. The expression of VCBP-C can be detected from the earliest stages of development; VCBP-C and bacteria both bind and colocalize to the resulting chitin-rich mucus matrix. In chordate taxa that diverged before the evolutionary emergence of adaptive immunity, soluble immune mediators encoding V-type immunoglobulin domains likely serve a role in the establishment and maintenance of gut homeostasis by modulating bacterial community structure

Methods

Results

Conclusion