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

Abstract

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 pathogenVibrio choleraein conditions mimicking its marine habitat. Prior reports have noted the occurrence of cellular filamentation inV. cholerae, with variable propensity to filament among both toxigenic and nontoxigenic strains. Using a filamenting strain ofV. choleraeO139, we show that cells with this morphotype gain a profound competitive advantage in colonizing and spreading on particles of chitin, the material many marineVibriospecies depend on for growth in seawater. Furthermore, filamentous cells can produce biofilms that are independent of primary secreted components of theV. choleraebiofilm 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-secretingV. choleraevariants, 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.

A Conserved Regulatory Circuit Controls Large Adhesins in Vibrio cholerae

“…To test for biofilm growth on chitin, we used a customized microfluidic assay in which pieces of chitin (sterilized shrimp shell) were immobilized, colonized with V. cholerae inoculum, and perfused with a defined seawater medium (61, 62). Attachment and subsequent biofilm growth on the chitin can then be quantified using confocal microscopy (Fig.…”

The Effects of Eugenol, Trans-Cinnamaldehyde, Citronellol, and Terpineol on Escherichia coli Biofilm Control as Assessed by Culture-Dependent and -Independent Methods

“…Interestingly, filamentous E. coli cells were observed to deform upon hydrodynamic forces as investigated in a microfluidic device, regardless of whether they were growing or non-growing cells due to their plasticity [42]. In turn, it was shown that cells of Vibrio cholerae filamenting strain gained a competitive advantage in colonizing and spreading on particles of chitin, the material Vibrio species depend on for growth [43]. Filamentation allowed the creation of a mesh network of cells through physical entanglement and independent of cell-cell adhesion components and the major polysaccharide for the V. cholerae biofilm matrix.…”

Biofilms 2018: a Diversity of Microbes and Mechanisms

“…To address the issue of which forces promote and maintain diversity in biofilms, Katrina Harris (laboratory of Vaughn Cooper, University of Pittsburgh, Pittsburgh, PA) described an evolution study in which biofilm-grown P. aeruginosa became highly diverse within 600 generations, with the diversity driven at least partially by the high frequency of appearance of mutator strains (8). Carey Nadell (Dartmouth College, Hanover, NH) described the ability of some V. cholerae strains to form filamentous cells that were capable of wrapping around and colonizing chitin fragments more efficiently than nonfilamentous V. cholerae (9). This ability was independent of known biofilm factors such as the vps polysaccharide locus and may confer an advantage in the environment, permitting V. cholerae to colonize chitinous surfaces such as crustaceans.…”