Transitions to multicellularity: the physical environment at the microscale
19 January 2023
Physical environment contribute to both the robustness and the variation of developmental trajectories and, eventually, to the evolutionary transitions. But how? Myxococcus xanthus is a soil bacterium and is widely used as a biological model. In starvation conditions, cells move individually over the substrate into growing groups of cells which, eventually, organize into three-dimensional structures called fruiting bodies. Commonly, this developmental process is studied using standard experimental protocols that employ homogeneous and flat agar substrates, without considering ecologically relevant variables. However M. Xanthus has shown to drastically alter its development when modifying variables such as the substrate topography or stiffness. This modifications occur with trait and scale specificity, at the level of individual cells, large group of cells, fruiting bodies and also at the population scale. We use experimental and analytical tools to study how multicellular organization is altered at different spatial scales and developmental moments.
The environment topography alters the transition from single-cell populations to multicellular structures in Myxococcus xanthus
Karla C. Hernández Ramos, Edna Rodríguez-Sánchez, Juan Antonio Arias del Angel, Alejandro V. Arzola, Mariana Benítez, Ana E. Escalante, Alessio Franci, Giovanni Volpe, Natsuko Rivera-Yoshida
Sci. Adv. 7(35), eabh2278 (2021)
The social soil-dwelling bacteria Myxococcus xanthus can form multicellular structures, known as fruiting bodies. Experiments in homogeneous environments have shown that this process is affected by the physico-chemical properties of the substrate, but they have largely neglected the role of complex topographies. We experimentally demonstrate that the topography alters single-cell motility and multicellular organization in M. xanthus. In topographies realized by randomly placing silica particles over agar plates, we observe that the cells’ interaction with particles drastically modifies the dynamics of cellular aggregation, leading to changes in the number, size and shape of the fruiting bodies, and even to arresting their formation in certain conditions. We further explore this type of cell-particle interaction in a minimal computational model. These results provide fundamental insights into how the environment topography influences the emergence of complex multicellular structures from single cells, which is a fundamental problem of biological, ecological and medical relevance.