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

Abstract

Columnaris disease is responsible for substantial losses throughout the production of many freshwater fish species. One of the ways in which the bacterium Flavobacterium columnare is so effective in initiating disease is through the formation of biofilms on fish skin and gills. To further explore the interaction between host factors and bacterial cells, we assayed the ability of vertebrate mucus to enhance F. columnare biofilm development. Different concentrations of catfish, tilapia and pig mucus (5–60 µg/ml) increased biofilm growth at varying degrees among F. columnare isolates. Our data suggest that vertebrate mucus acts as a signalling molecule for the development of F. columnare biofilms; however, there are clear disparities in how individual isolates respond to different mucus fractions to stimulate biofilms. The expression of iron acquisition genes among two genomovar II isolates showed that ferroxidase, TonB receptor and the siderophore synthetase gene were all significantly upregulated among F. columnare biofilms. Interestingly, the siderophore acetyltransferase gene was only shown to be significantly upregulated in one of the genomovar II isolates. This work provides insight into our understanding of the interaction between F. columnare and vertebrate mucus, which likely contributes to the growth of planktonic cells and the transition into biofilms.

Differential susceptibility of white bass (Morone chrysops), striped bass (Morone saxatilis) and hybrid striped bass (M. chrysops × M. saxatilis) to Flavobacterium columnare and effects of mucus on bacterial growth and biofilm development

“…There is likely a multi‐faceted mechanism involving factors such as microbiome, nutritional state, environmental status, genetics or physiological factors that affect susceptibility to pathogens among moronid species, similar to what has been demonstrated in Ictalurid species (Geng et al., 2015). Additionally, this study only utilized one F. columnare isolate; therefore, it is plausible other isolates may react differently to exposure to moronid mucus; however, this isolate was previously used to evaluate differential susceptibilities in moronids (Fuller et al., 2014), and has been well characterized in other studies (Beck et al., 2015; Lange et al., 2017, 2020).…”

“…Fish mucus is an important defence against bacterial pathogens, and the mucosal layer offers protection against the surrounding aquatic environment (Ben Hamed et al., 2018; Benhamed et al., 2014). Further, it has been demonstrated that fish mucus may act as a nutritive source for some F. columnare isolates (Shoemaker & Lafrentz, 2015; Shoemaker et al., 2018), and F. columnare planktonic cells have displayed chemotaxis to fish mucus (Klesius et al., 2008; LaFrentz & Klesius, 2009; Lange et al., 2020).…”

Cadmium sulfide nanoparticle biomineralization and biofilm formation mediate cadmium resistance of the deep‐sea bacterium Pseudoalteromonas sp. MT33b

“…Of note, bacteria secretion and TonB‐dependent transfer system are involved in the DNA/protein secretion and iron (Fe) transport (Fig. S9) (Koebnik, 2005; Perraud et al ., 2020; Zhai et al ., 2021) respectively, which are all proposed to be closely related to biofilm formation (Dong et al ., 2019; Lange et al ., 2020; Zhang et al ., 2020). Compared with Cd group, genes related to exopolysaccharide synthesis were upregulated in CysCd group (Fig.…”

“…4D), indicating that Pseudoalteromonas sp. MT33b, similar to the previous reports (Dong et al ., 2019; Lange et al ., 2020), might enable to upregulate the absorption and transport of iron, thereby promoting iron storage and the formation of biofilms. Consistently, the marine heterotroph Pseudoalteromonas has been reported to possess expansive iron storage capacity and utilization strategies despite the extreme scarcity of iron in seawater (Mazzotta et al ., 2020).…”

Phenolic substances as regulators of the intensity of lipid peroxidation processes of the strains Pleurotus eryngii, Fistulina hepatica and Agrocybe cylindracea

“…Among the most common diseases, a special place is occupied by columnaris, which is recognized as a serious threat to the health of both wild and cultured freshwater fish (Lange et al, 2019(Lange et al, , 2020Tan et al, 2019). The disease is accompanied by high mortality and causes significant losses in aquaculture (Meepagala et al, 2018;Kitiyodom et al, 2019).…”