Sickeningly Sweet: L‐rhamnose stimulates Flavobacterium columnare biofilm formation and virulence

Abstract

Flavobacterium columnare, the causative agent of columnaris disease, causes substantial mortality worldwide in numerous freshwater finfish species. Due to its global significance and impact on the aquaculture industry continual efforts to better understand basic mechanisms that contribute to disease are urgently needed. The current work sought to evaluate the effect of L-rhamnose on the growth characteristics of F. columnare. While we initially did not observe any key changes during the total growth of F. columnare isolates tested when treated with L-rhamnose, it soon became apparent that the difference lies in the ability of this carbohydrate to facilitate the formation of biofilms. The addition of different concentrations of L-rhamnose consistently promoted the development of biofilms among different F. columnare isolates; however, it does not appear to be sufficient as a sole carbon source for biofilm growth. Our data also suggest that iron acquisition machinery is required for biofilm development. Finally, the addition of different concentrations of L-rhamnose to F. columnare prior to a laboratory challenge increased mortality rates in channel catfish (Ictalurus punctatus) as compared to controls. These results provide further evidence that biofilm formation is an integral virulence factor in the initiation of disease in fish.

Vertebrate mucus stimulates biofilm development and upregulates iron acquisition genes in Flavobacterium columnare

“…They concluded that the different carbohydrate receptors likely incorporated into the catfish mucus acted as bacterial chemoattractants. We reached a similar conclusion after demonstrating that in vitro biofilm formation was enhanced when stimulated with the carbohydrate, L‐rhamnose (Lange et al, ). We had also previously posited that the ability to form robust biofilms correlated with an ability to cause significant disease.…”

“…However, when we examined the effect of catfish mucus on biofilm formation, it was shown that mucus alone was unable to drive the development of in vitro biofilms. Therefore, similar to a previous conclusion when evaluating the carbohydrate L‐rhamnose, fish mucus does not appear to be used solely as a nutrition source in the development of biofilms (Lange et al, ). Another possibility is that very little biofilm growth was observed in “mucus alone” due to limited nutritive iron availability in the mucus fractions (Hunter et al, ).…”

“…There is not a shortage of studies, which link the importance of acquiring free iron in the successful development of Gram‐negative biofilms (Cornelis, Matthijs, & Van Oeffelen, ; Kang & Kirienko, ). Our data suggest that iron acquisition is an important component in establishing biofilms and that F. columnare isolates likely utilize different uptake pathways to retain iron (Lange et al, , ). Alternatively, much of the work to examine environmental and dietary iron uptake mechanisms in teleost fish has focused on the intestinal and gill mucus membranes (Bury, ; Bury, Walker, & Glover, ; Cooper, Handy, & Bury, ).…”

The role of rpoS in the regulation of Vibrio alginolyticus virulence and the response to diverse stresses

“…Biofilm formation could enhance the resistance to antibiotics (Khandekar et al., ; Yatip, Teja, Flegel, & Soowannayan, ) and host immune killing (Abdallah, Mahmoud, & Abdel‐Rahim, ; Chenia & Duma, ; Lange et al., ), while biofilm formation of Vibrio depends on complex regulatory processes (Cai et al., ). rpoS is involved in biofilm production in several bacteria, such as E. coli , Pseudomonas aeruginosa and Edwardsiella tarda (Xiao et al., ), although no such research about V. alginolyticus has yet been reported.…”

Influence of native catfish mucus on Flavobacterium columnare growth and proteolytic activity

“…Limited research has examined the terminal carbohydrate composition of fish mucus even though pathogen contact, and adhesion is often mediated by bacterial lectin receptors and/or host lectin receptors that bind to the sugars expressed by pathogens and/or at mucosal surfaces (Beck et al., ; Lange et al., ; Tse & Chadlee, ). All lectins tested bound to the mucus of channel and hybrid catfish albeit some with greater affinity that included Concavalia ensiformis lectin (conA), Lycopersicon esculentum lectin (LEA) and Triticum vulgaris lectin (WGA) in the greatest abundance (Figure ).…”