Understanding the Complexity of Mucosal Immunity in Channel Catfish (Ictalurus punctatus)

Abstract

The mucosal surfaces of fish (gill, skin, intestine) serve as the first line of defense against a myriad of aquatic pathogens. Although interest in understanding components of the mucosal immune response in fish is growing, little is known about how host mucosal molecular and cellular constituents may impact rates of pathogen adhesion and tissue invasion. The freshwater bacterial pathogens Edwardsiella ictaluri, Aeromonas hydrophila and Flavobacterium columnare infect a variety of farmed fish species worldwide through various mucosal attachment points. The availability of transcriptomic tools including microarrays and RNA-Seq has recently opened a window through which we can observe the complexity of fish host-pathogen interactions during infection. In order to characterize the immune actors and events taking place at the mucosal surfaces and identify the routes of pathogen attachment and entry, RNA-seq and microarray approaches were utilized to broadly investaged the transcriptional effects during bacterial infection in channel catfish. E.ictaluri is believed to gain entry through the intestinal epithelium. Following E. ictaluri challenge, the RNA-seq observed differentially expressed genes set indicated the centrality of actin cytoskeletal polymerization and junctional regulation in pathogen entry and subsequent inflammatory responses. A successful A. hydrophila infection always starts with the disturbed skin. At critical early timepoints following challenge in the skin, microarray analyses found that A. hydrophila infection rapidly altered a number of mucosal factors in a manner predicted to enhance its ability to adhere to and invade the catfish host. Adhesion of F. columnare to gill tissue is correlated to virulence and host susceptibility. Here, the observed immune and mucin profiles between channel catfish differing in their susceptibility to F. columnare both before infection and at three early timepoints post-infection suggested a basal polarization in the gill mucosa. As the fasting impacts susceptibility to F.columnare, in gill and skin 7 day fasting significantly altered expression of critical innate immune factors. Taken together, our results set a foundation for future studies comparing mechanisms of mucosal immunity across several important catfish pathogens. Understanding of molecular mechanisms of pathogen entry during infection will provide insight into strategies for selection of resistant catfish brood stocks against various diseases.