Gliding motility of a uranium tolerant Bacteroidetes bacterium Chryseobacterium sp. strain PMSZPI: Insights into the architecture of spreading colonies

Abstract

SummaryUranium tolerant soil bacterium Chryseobacterium sp. strain PMSZPI moved over solid agar surfaces by gliding motility thereby forming spreading colonies which is a hallmark of members of Bacteroidetes phylum. PMSZPI genome harbored orthologs of all the gld and spr genes considered as core bacteroidetes gliding motility genes of which gldK, gldL, gldM, and gldN were co-transcribed. Here, we present the intriguing interplay between gliding motility and cellular organization in PMSZPI spreading colonies. While nutrient deficiency enhanced colony spreading, high agar concentrations and presence of motility inhibitor like 5-hydroxyindole reduced the spreading. A detailed in situ structural analysis of spreading colonies revealed closely packed cells forming multiple layers at center of colony while the edges showed clusters of cells periodically arranged in hexagonal lattices interconnected with each other. The cell migration within the colony was visualized as branched structures wherein the cells were buried within extracellular matrix giving rise to ‘fern’ like patterns. PMSZPI colonies exhibited strong iridescence that showed correlation with gliding motility. Presence of uranium reduced motility and iridescence and induced biofilm formation. This is a first report of gliding motility and iridescence in a bacterium from uranium enriched environment that could be of significant interest from an ecological perspective.Originality-Significance StatementThis work provides the first description of the gliding motility and iridescence or structural coloration in a Bacteroidetes soil bacterium from uranium enriched environment. The periodic arrangement of the cell population in the spreading colonies achieved through gliding motility resulted in bright structural coloration of the colonies when illuminated. The study describes the exogenous factors including nutrition, substrate, presence of uranium influencing the motility and iridescence of the bacterium. The highly organized cell population in the gliding and iridescent bacterium may have conferred survival advantage in metal/uranium enriched ecosystem.