Abstract
The second messenger signaling molecule cyclic diguanylate monophosphate (c-di-GMP) drives the transition between planktonic and biofilm growth in many bacterial species. Pseudomonas aeruginosa has two surface sensing systems that produce c-di-GMP in response to surface adherence. Current thinking in the field is that once cells attach to a surface, they uniformly respond by producing c-di-GMP. Here, we describe how the Wsp system generates heterogeneity in surface sensing, resulting in two physiologically distinct subpopulations of cells. One subpopulation has elevated c-di-GMP and produces biofilm matrix, serving as the founders of initial microcolonies. The other subpopulation has low c-di-GMP and engages in surface motility, allowing for exploration of the surface. We also show that this heterogeneity strongly correlates to surface behavior for descendent cells. Together, our results suggest that after surface attachment, P. aeruginosa engages in a division of labor that persists across generations, accelerating early biofilm formation and surface exploration.
Highlights
Pseudomonas aeruginosa is an opportunistic pathogen that engages in a range of surface-associated behaviors and is a model bacterium for studies of surface-associated communities called biofilms
Our data show that heterogeneity in cellular levels of c-di-GMP generated by the Wsp system in response to surface sensing, leads to two physiologically distinct subpopulations that each contribute to surface colonization
Phenotypic heterogeneity of single cells is a common phenomenon in bacteria that can be beneficial at the population level by allowing a single genotype to survive sudden environmental changes
Summary
Pseudomonas aeruginosa is an opportunistic pathogen that engages in a range of surface-associated behaviors and is a model bacterium for studies of surface-associated communities called biofilms. Bacteria in biofilms have long been appreciated to exhibit phenotypic heterogeneity due to chemical variation within the biofilm itself, including gradients of oxygen (Wessel et al, 2014), nutrients (Schreiber et al, 2016), and pH (Vroom et al, 1999) These environmental conditions are sensed by individual bacterial cells, leading to differential gene expression and metabolic activities even within a genetically homogeneous population (Stewart and Franklin, 2008). Within a clonal population of P. aeruginosa, we found that levels of c-di-GMP vary among individual cells as they sense a surface, leading to a division of labor between two energetically costly behaviors associated with early biofilm formation: surface exploration and polysaccharide production
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