Differential interaction forces govern bacterial sorting in early biofilms

Bacterial biofilms can generate micro-heterogeneity in terms of surface structures. However, little is known about the associated changes in the physics of cell–cell interaction and its impact on the architecture of biofilms. In this study, we used the type IV pilus of Neisseria gonorrhoeae to test whether variation of surface structures induces cell-sorting. We show that the rupture forces between pili are fine-tuned by post-translational modification. Bacterial sorting was dependent on pilus post-translational modification and pilus density. Active force generation was necessary for defined morphologies of mixed microcolonies. The observed morphotypes were in remarkable agreement with the differential strength of adhesion hypothesis proposing that a tug-of-war among surface structures of different cells governs cell sorting. We conclude that in early biofilms the density and rupture force of bacterial surface structures can trigger cell sorting based on similar physical principles as in developing embryos. DOI: http://dx.doi.org/10.7554/eLife.10811.001
eLife digest Communities of bacterial cells can live together embedded within a slime-like molecular matrix as a biofilm. This allows the bacteria to hide from external stresses. A single bacterium can replicate itself and develop into a biofilm, and over time the bacterial cells in specific regions of the biofilm will start to interact with their neighbors in different ways. These interactions occur via structures on the surface of the bacterial cells, and the differences in these interactions resemble those that occur as cells specialize during the development of animal embryos. Previous research into embryonic development has shown how differences in the physical interactions between embryonic cells are essential for sorting the cells into their correct locations and shaping the embryo. However, little is known about which processes govern the development of biofilms. Now, Oldewurtel et al. have asked whether differences in the physical interactions between bacteria trigger cell sorting during the early stages of biofilm development. The experiments involved measuring the force required to break the cell–cell connections (called the ‘rupture force’) in biofilms of a bacterium called Neisseria gonorrhoeae. Oldewurtel et al. found that, in agreement with previous predictions, physical interactions were important for sorting bacterial cells into clusters based on the structures on their surfaces. Bacterial cells actively pull on the surface structures of their neighbors, which allows the cells to sort themselves in a tug-of-war fashion. This means that a cell will move in the direction where it can pull the strongest (i.e., in the direction where the rupture force is highest). While bacteria and embryos use different molecules to generate these pulling forces, these findings indicate that the basic physical principles are similar in both systems. One of the next challenges will be to evaluate how biofilms might benefit from the structures that develop due to cell sorting. DOI: http://dx.doi.org/10.7554/eLife.10811.002