Interconnected Cavernous Structure of Bacterial Fruiting Bodies

The formation of spore-filled fruiting bodies by myxobacteria is a fascinating case of multicellular self-organization by bacteria. The organization of Myxococcus xanthus into fruiting bodies has long been studied not only as an important example of collective motion of bacteria, but also as a simplified model for developmental morphogenesis. Sporulation within the nascent fruiting body requires signaling between moving cells in order that the rod-shaped self-propelled cells differentiate into spores at the appropriate time. Probing the three-dimensional structure of myxobacteria fruiting bodies has previously presented a challenge due to limitations of different imaging methods. A new technique using Infrared Optical Coherence Tomography (OCT) revealed previously unknown details of the internal structure of M. xanthus fruiting bodies consisting of interconnected pockets of relative high and low spore density regions. To make sense of the experimentally observed structure, modeling and computer simulations were used to test a hypothesized mechanism that could produce high-density pockets of spores. The mechanism consists of self-propelled cells aligning with each other and signaling by end-to-end contact to coordinate the process of differentiation resulting in a pattern of clusters observed in the experiment. The integration of novel OCT experimental techniques with computational simulations can provide new insight into the mechanisms that can give rise to the pattern formation seen in other biological systems such as dictyostelids, social amoeba known to form multicellular aggregates observed as slugs under starvation conditions. Author Summary: Understanding bacteria self-organization is an active area of research with broad implications in both microbiology and developmental biology. Myxococcus xanthus undergoes multicellular aggregation and differentiation under starvation and is widely used as a model organism for studying bacteria self-organization. In this paper, we present the findings of an innovative non-invasive experimental technique that reveals a heterogeneous structure of the fruiting body not seen in earlier studies. Insight into the biological mechanism for these observed patterns is gained by integrating experiments with biologically relevant computational simulations. The simulations show that a novel mechanism requiring cell alignment, signaling and steric interactions can explain the pockets of spore clusters observed experimentally in the fruiting bodies of M. xanthus.