ARS | Publication request: Rhamnose-binding lectins and their ligands: Putative roles in Flavobacterium columnare pathogenesis in channel catfish Ictalurus punctatus

Submitted to: Fish and Shellfish Immunology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: August 17, 2012
Publication Date: October 1, 2012
Citation: Beck, B.H., Farmer, B.D., Straus, D.L., Li, C., Peatman, E. 2012. Rhamnose-binding lectins and their ligands: Putative roles in Flavobacterium columnare pathogenesis in channel catfish Ictalurus punctatus. Fish and Shellfish Immunology. 33(4):1008-1015.

Interpretive Summary: Columnaris disease is a bacterial disease of channel catfish that causes large economic losses to catfish farmers. Despite the importance of this disease, little is known about how the bacteria infects the fish and causes disease. This study examined a group of molecules found in the catfish gill (one of the main organs affected by columnaris disease) called rhamnose-binding lectins (RBL). The RBLs are a part of the immune system and function by attaching to the surface of bacteria, which assists other parts of the immune system in the killing of the bacteria. After exposure to columnaris disease, we examined the levels of RBL in the gill of two different families of channel catfish; one family was known to be susceptible to columnaris disease, while the other was completely resistant. Contrary to what was expected, we found that the amount of RBL present in the gill was strongly increased in the columnaris-susceptible family of channel catfish but not the resistant. Next, by reducing the number of RBL binding sites on the gill, we found that channel catfish could be protected from columnaris disease. Lastly, we found that RBL levels were tightly controlled by the nutritional status of the fish, with a far greater amount of RBL present in the gill of unfed fish relative to well-fed fish. This research represents a novel approach to addressing one of the major disease problems afflicting cultured catfish. Catfish producers and consumers will greatly benefit from the economic returns associated with reducing costly production losses due to columnaris disease.

Technical Abstract: Columnaris disease, caused by the bacterial pathogen Flavobacterium columnare, continues to be a major problem worldwide and commonly leads to tremendous losses of both wild and cultured freshwater fish, particularly in intensively farmed aquaculture species such as channel catfish. Despite its ecologic and economic impacts, the fundamental molecular mechanisms of the host immune response to this pathogen remain unclear. While F. columnare can induce marked pathologic changes in numerous ectopic tissues, the adhesion of F. columnare to the gill in particular is strongly associated with pathogen virulence and host susceptibility. Recently, in this regard, using RNA-seq expression profiling we found that a rhamnose-binding lectin (RBL) was dramatically upregulated in the gill of fish infected with F. columnare (as compared to naïve fish). Thus, in the present study we sought to further characterize and understand the RBL response in channel catfish. We first identified two distinct catfish families with differential susceptibilities to columnaris disease; one family was found to be completely resistant while the other was susceptible (0% mortality versus 18.3 % respectively, P < 0.001). Exclusively, in the susceptible family, we observed an acute and robust upregulation in catfish RBL that persisted for at least 24h (P < 0.05). To elucidate whether RBL play a more direct role in columnaris pathogenesis, we exposed channel catfish to different doses of the putative RBL ligands L-rhamnose and D-galactose, and found that these sugars, protected channel catfish against columnaris disease, likely through competition with F. columnare binding of host RBL. Finally, we examined the role of nutritional status on RBL regulation and found that RBL expression was upregulated (>55-fold; P < 0.05) in fish fasted for 7 d (as compared to fish fed to satiation daily), yet expression levels returned to those of satiated fish within 4 h after re-feeding. Collectively, these findings highlight putative roles for RBL in the context of columnaris disease and reveal new aspects linking RBL regulation to feed availability.