Short-Term Feed Deprivation Alters Immune Status of Surface Mucosa in Channel Catfish (Ictalurus punctatus)

Abstract

Short-term feed deprivation (or fasting) is a common occurrence in aquacultured fish species whether due to season, production strategies, or disease. In channel catfish (Ictalurus punctatus) fasting impacts susceptibility to several bacterial pathogens including Flavobacterium columnare, the causative agent of columnaris disease. As columnaris gains entry through the gills and skin of fish, we examined here changes in transcriptional regulation induced in these surface mucosal tissues due to short-term (7 day) fasting. RNA-seq expression analysis revealed a total of 1,545 genes perturbed by fasting. Fasting significantly altered expression of critical innate immune factors in a manner consistent with lower immune fitness as well as dysregulating key genes involved in energy metabolism and cell cycling/proliferation. Downregulation of innate immune actors such as iNOS2b, Lysozyme C, and peptidoglycan recognition protein 6 is predicted to impact the delicate recognition/tolerance balance for commensal and pathogenic bacteria on the skin and gill. The highlighted expression profiles reveal potential mechanistic similarities between gut and surface mucosa and underscore the complex interrelationships between nutrition, mucosal integrity, and immunity in teleost fish.

Physiology and immunology of mucosal barriers in catfish (Ictalurus spp.)

“…Yazawa et al 55 established a transgenic zebrafish strain expressing a chicken lysozyme gene under the control of a keratin promoter which resulted in a 65% survival rate against F.columnare compared to 0% survival in wild-type fish. 25 We have also observed suppression of skin/gill lysozyme C levels following short-term feed deprivation 30 and elevated lysozyme levels in gills following feeding a diet supplemented with mannan-oligosaccharides (unpublished results).…”

“…3 A series of RNA-seq expression studies in catfish gill exposed to F. columnare or following feed deprivation have cataloged a diverse innate repertoire likely secreted into the mucus. 25,30,47 These include complement factor D, C1, C7, C1q, NK-lysin, bacterial permeability-increasing protein (BPI) and several fish toxin proteins including natterin and toxin-1 precursor, lysozyme C, and lysozyme G. In the intestine, we have additionally detected H2 antimicrobial peptides, serine proteases, granzyme and abundant metalloproteinases. 44 Of these, lysozyme C appears to be a particularly good marker of immune readiness, particularly in the skin and gill of catfish.…”

“…As mentioned above, short-term feed deprivation in channel catfish altered mucin expression in both skin and gill, potentially through changes in gene expression of AGR2. 30 A similar fasting study in blue catfish revealed drastically different levels of mucin expression, potentially altering the host-pathogen dynamics in host fish. 29 In recent years a virulent strain of Aeromonas hydrophila capable of producing a motile aeromonad septicemia (MAS) infection, has caused widespread mortality in the US catfish industry.…”

“…[26][27][28] Mucin levels are also altered by short-term fasting, a nutritional state previously associated with higher F. columnare mortality. [29][30][31] Goblet cell proliferation appears to be under the control of anterior gradient 2 protein (AGR2) in zebrafish. 32 Similarly, we have observed changes in AGR2 due to diet and immune status.…”

“…32 Similarly, we have observed changes in AGR2 due to diet and immune status. 25,30 Quantity and composition (e.g. sialomucin vs. sulfomucin) of mucus is likely critical for dynamics of pathogen invasion, successful attachment to host receptors, and persistence, and, therefore, is a target of immuno-sculpting by fish pathogens.…”