Evidence that the stress hormone cortisol regulates biofilm formation differently among Flavobacterium columnare isolates

Authors: DECLERCQ, A.M. - Ghent University; CAI, C. - Auburn University; NARANJO, W. - Auburn University; THONGDA, W. - Auburn University; EECKHAUT, V. - Ghent University; BAUWENS, E. - Ghent University; ARIAS, C. - Auburn University; DE LA FUENTE, L. - Auburn University; Beck, Benjamin; Lange, Miles; PEATMAN, ERIC - Auburn University; AERTS, J. - Ghent University; HAESEBROUCK, F. - Ghent University; DECOSTERE, A. - Ghent University

Submitted to: Veterinary Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/26/2019
Publication Date: 4/11/2019
Citation: Declercq, A., Cai, C., Naranjo, W., Thongda, W., Eeckhaut, V., Bauwens, E., Arias, C., De La Fuente, L., Beck, B.H., Lange, M.D., Peatman, E., Aerts, J., Haesebrouck, F., Decostere, A. 2019. Evidence that the stress hormone cortisol regulates biofilm formation differently among Flavobacterium columnare isolates. Veterinary Research. 50(1):24. https://doi.org/10.1186/s13567-019-0641-3.
DOI: https://doi.org/10.1186/s13567-019-0641-3

Interpretive Summary: The impact of the stress hormone cortisol on biofilm formation by Flavobacterium columnare, the causative agent of columnaris disease, was evaluated. First, the dynamics of biofilm formation by a highly (HV) and low virulent (LV) F. columnare isolate supplemented with/without a high dose of cortisol under microfluidic flow (a chamber designed to model the gill environment) conditions was characterized. In both isolates, cell aggregates resembling biofilms occurred within 7-h post-inoculation. Consequently, cell clusters were sloughed away, immediately followed by a rebuilding of bacterial cell aggregates, occurring four times and once in the 24-h observation period for the HV and LV isolate, respectively, possibly indicating the higher spreading capacity of the former. The LV isolate only revealed upstream cell aggregates upon cortisol supplemention. Secondly, the expression of genes was investigated in planktonic and biofilm cells of a HV and LV isolate to which no, a low or high dose of cortisol was added. Significantly less expression of gliding genes was seen in the planktonic cells of the LV isolate supplemented with a high cortisol dose. The LV isolate biofilm cells treated with the high cortisol dose showed a significant upregulation of genes encoding mobility and surface adhesion proteins. This is the first proof of the co-regulatory effect of cortisol in biofilm formation and expression of gliding genes in F. columnare, thereby launching new research perspectives for microbial endocrinology.

Technical Abstract: The impact of cortisol on biofilm formation by Flavobacterium columnare, the causative agent of columnaris disease, was evaluated. Firstly, the dynamics of biofilm formation by a highly (HV) and low virulent (LV) F. columnare isolate supplemented with no/a high dose of cortisol under microfluidic flow conditions was characterized. In both isolates, - cell aggregates resembling biofilms occurred within 7-h post-inoculation. Consequently, cell clusters were sloughed away, immediately followed by a rebuilding of bacterial cell aggregates, occurring four times and once in the 24-h observation period for the HV and LV isolate, respectively, possibly indicating the higher spreading capacity of the former. The LV isolate only revealed counter-current cell aggregates upon cortisol supplemention. Secondly, the expression of genes belonging to the TypeIX secretion system (gldK, gldL, gldM, gldN, porV, sprA, sprB, sprE, sprT, and porV) was investigated in planktonic and biofilm cells of a HV and LV isolate to which no, a low or high dose of cortisol was added. Significantly less expression of gliding genes gldK, gldL, gldM and gldN, and of protein secretion regulator porV was seen in the planktonic cells of the LV isolate supplemented with a high cortisol dose. The LV isolate biofilm cells treated with the high cortisol dose showed a significant upregulation of sprT,and of sprB, encoding mobile surface adhesion important in bacterial colonization. This is the first proof of the co-regulatory effect of cortisol in biofilm formation and expression of gliding genes in F. columnare, thereby launching new research perspectives for microbial endocrinology.