Abstract

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.

Highlights

  • The organization of Myxococcus xanthus, the most studied species of the myxobacteria, into structures known as fruiting bodies has long been studied as an example of collective motion of bacteria, and as a simplified model for developmental morphogenesis [1,2]

  • In this paper, an integrative approach that combines a new experimental technique using infra-red optical coherence tomography (OCT) with computational models to study the patterns of spores as they form within a fruiting body

  • 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

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Summary

Introduction

The organization of Myxococcus xanthus, the most studied species of the myxobacteria, into structures known as fruiting bodies has long been studied as an example of collective motion of bacteria, and as a simplified model for developmental morphogenesis [1,2]. The cells differentiate from motile rod shaped cells to non-motile spherical spores that can wait out the harsh conditions. During this process, a 17 kD protein known as C-signal is transferred between cells and critical to the differentiation process [5,6]. It has been shown that C-signal requires end-to-end alignment [5], that C-signaling requires cells to move[7], and that C-signal accumulates on cells throughout development process and peaks when spores form [8]

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