Vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms

Significance The human pathogen Vibrio cholerae, when not inside of a host, grows in cell clusters (biofilms) on pieces of detritus in aquatic environments. Here we discovered that some isolates of V. cholerae can change their shape from small comma-shaped cells to long filaments in seawater. This altered cell shape allows cells to make new types of biofilms, and provides an advantage in quickly colonizing particles in seawater, at the expense of longer-term competitive ability. The filamentous cell-shape strategy is particularly effective at competing in environments with quick turnover of chitin particles. This result showcases how bacterial cell shape can be coupled to environmental success during surface occupation, competition within biofilms, and dispersal to new resource patches.
Collective behavior in spatially structured groups, or biofilms, is the norm among microbes in their natural environments. Though biofilm formation has been studied for decades, tracing the mechanistic and ecological links between individual cell morphologies and the emergent features of cell groups is still in its infancy. Here we use single-cell–resolution confocal microscopy to explore biofilms of the human pathogen Vibrio cholerae in conditions mimicking its marine habitat. Prior reports have noted the occurrence of cellular filamentation in V. cholerae, with variable propensity to filament among both toxigenic and nontoxigenic strains. Using a filamenting strain of V. cholerae O139, we show that cells with this morphotype gain a profound competitive advantage in colonizing and spreading on particles of chitin, the material many marine Vibrio species depend on for growth in seawater. Furthermore, filamentous cells can produce biofilms that are independent of primary secreted components of the V. cholerae biofilm matrix; instead, filamentous biofilm architectural strength appears to derive at least in part from the entangled mesh of cells themselves. The advantage gained by filamentous cells in early chitin colonization and growth is countered in long-term competition experiments with matrix-secreting V. cholerae variants, whose densely packed biofilm structures displace competitors from surfaces. Overall, our results reveal an alternative mode of biofilm architecture that is dependent on filamentous cell morphology and advantageous in environments with rapid chitin particle turnover. This insight provides an environmentally relevant example of how cell morphology can impact bacterial fitness.