Motility Enhancement through Surface Modification Is Sufficient for Cyanobacterial Community Organization during Phototaxis

The emergent behaviors of communities of genotypically identical cells cannot be easily predicted from the behaviors of individual cells. In many cases, it is thought that direct cell-cell communication plays a critical role in the transition from individual to community behaviors. In the unicellular photosynthetic cyanobacterium Synechocystis sp. PCC 6803, individual cells exhibit light-directed motility (“phototaxis”) over surfaces, resulting in the emergence of dynamic spatial organization of multicellular communities. To probe this striking community behavior, we carried out time-lapse video microscopy coupled with quantitative analysis of single-cell dynamics under varying light conditions. These analyses suggest that cells secrete an extracellular substance that modifies the physical properties of the substrate, leading to enhanced motility and the ability for groups of cells to passively guide one another. We developed a biophysical model that demonstrates that this form of indirect, surface-based communication is sufficient to create distinct motile groups whose shape, velocity, and dynamics qualitatively match our experimental observations, even in the absence of direct cellular interactions or changes in single-cell behavior. Our computational analysis of the predicted community behavior, across a matrix of cellular concentrations and light biases, demonstrates that spatial patterning follows robust scaling laws and provides a useful resource for the generation of testable hypotheses regarding phototactic behavior. In addition, we predict that degradation of the surface modification may account for the secondary patterns occasionally observed after the initial formation of a community structure. Taken together, our modeling and experiments provide a framework to show that the emergent spatial organization of phototactic communities requires modification of the substrate, and this form of surface-based communication could provide insight into the behavior of a wide array of biological communities.Author Summary: Communities of bacterial cells exhibit social behaviors that single cells cannot engage in alone. These behaviors are often a product of direct interactions that allow cells to communicate with each other. In the unicellular photosynthetic cyanobacterium Synechocystis, groups of cells collectively move along a surface toward a light source in characteristic, spatial patterns that do not seem to require that cells directly communicate or change their individual behavior. By varying the direction of the light source, we show experimentally that cells indirectly interact by secreting a substance that allows them to move more rapidly and to follow the paths left by other cells. We develop a biophysical model demonstrating that this form of interaction is sufficient to reproduce our experimental observations, and complement this model with simulations and physical scaling laws that provide a useful tool to design and interpret future experiments. Based on our results, we propose that physical modification of the cellular microenvironment may play an important role in inducing group behaviors in other systems.