Extracellular appendages govern spatial dynamics and growth of Caulobacter crescentus on a prevalent biopolymer

Abstract

Microbial breakdown of carbon polymers is an essential process in all ecosystems. Carbon polymers generally require extracellular breakdown by secreted exoenzymes. Exoenzymes and breakdown products can be lost through diffusion or flow. This diffusional loss is reduced when bacteria grow in surface-associated populations where they benefit from each others metabolic activities. The aquatic organism Caulobacter crescentus was recently shown to form clonal microcolonies on the carbon polymer xylan, but to grow solitary on the monosaccharide xylose. The underlying mechanisms of this substrate-mediated microcolony formation are unknown. In particular, the importance of extracellular appendages such as pili, adhesive holdfast, and flagellum in governing the spatial arrangement of surface-grown cells is unclear. Using microfluidics coupled to automated time-lapse microscopy and quantitative image analysis, we compared the temporal and spatial dynamics of C. crescentus wildtype and mutant strains grown on xylan, xylose, or glucose. We found that mutants lacking type IV pili or holdfast showed altered spatial patterns in microcolonies and were unable to maintain cell densities above a threshold required for maximal growth rates on the xylan polymer, whereas mutants lacking flagella showed increased cell densities that potentially lead to increased local competition. Our results demonstrate that extracellular appendages allow bacteria to reach local cell densities that maximize single-cell growth rates in response to their nutrient environment.