Abstract
Campylobacter is a leading foodborne pathogen worldwide. Biofilm formation is an important survival mechanism that sustains the viability of Campylobacter under harsh stress conditions. Iron affects biofilm formation in some other bacteria; however, the effect of iron on biofilm formation has not been investigated in Campylobacter. In this study, we discovered that ferrous (Fe2+) and ferric (Fe3+) iron stimulated biofilm formation in Campylobacter jejuni. The sequestration of iron with an iron chelator prevented the iron-mediated biofilm stimulation. The level of total reactive oxygen species (ROS) in biofilms was increased by iron. However, the supplementation with an antioxidant prevented the total ROS level from being increased in biofilms by iron and also inhibited iron-mediated biofilm stimulation in C. jejuni. This suggests that iron promotes biofilm formation through oxidative stress. Based on the results of fluorescence microscopic analysis, Fe2+ and Fe3+ enhanced both microcolony formation and biofilm maturation. The levels of extracellular DNA and polysaccharides in biofilms were increased by iron supplementation. The effect of iron on biofilm formation was also investigated with 70 C. jejuni isolates from raw chicken. Regardless of the inherent levels of biofilm formation, iron stimulated biofilm formation in all tested strains; however, there were strain variations in iron concentrations affecting biofilm formation. The biofilm formation of 92.9% (65 of 70) strains was enhanced by either 40 μM Fe2+ or 20 μM Fe3+ or both (the iron concentrations that enhanced biofilm formation in C. jejuni NCTC 11168), whereas different iron concentrations were required to promote biofilms in the rest of the strains. The findings in this study showed that Fe2+ and Fe3+ contributed to the stimulation of biofilm formation in C. jejuni through oxidative stress.
Highlights
Campylobacter is a leading bacterial cause of gastroenteritis and is responsible for approximately 166 million diarrheal cases and 37,600 deaths worldwide per year (Kirk et al, 2015)
In this study, we investigated the effect of ferrous (Fe2+) and ferric (Fe3+) iron on biofilm formation in C. jejuni NCTC 11168 and 70 C. jejuni strains isolated from raw chicken
The averages of bacterial counts in biofilms were slightly reduced at iron concentrations ≥20 μM, the reduction was not statistically significant, and the viability of C. jejuni in biofilms was not altered at the iron concentrations tested in the study (Supplementary Figure S1A)
Summary
Campylobacter is a leading bacterial cause of gastroenteritis and is responsible for approximately 166 million diarrheal cases and 37,600 deaths worldwide per year (Kirk et al, 2015). In addition to gastrointestinal infections, in some cases, Campylobacter jejuni may result in the development of Guillain–Barré syndrome (GBS), an acute flaccid paralysis (Willison et al, 2016). Biofilm Formation in Campylobacter animals (Huang et al, 2015), poultry is considered as the most important reservoir for foodborne transmission of C. jejuni to humans (Hermans et al, 2012). Compared to other foodborne pathogens, such as Salmonella and pathogenic Escherichia coli, C. jejuni is physiologically unique (e.g., microaerophilic and asaccharolytic) and fastidious to culture (Silva et al, 2011). Specific culture conditions are required for the growth of C. jejuni. C. jejuni requires CO2, and carbonic anhydrase that is encoded by canB contributes to C. jejuni growth under low (such as 1%) CO2 conditions (Al-Haideri et al, 2016)
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