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Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus

Nature volume 425, pages 75–78 (2003)Cite this article

Abstract

Cooperation among individuals is necessary for evolutionary transitions to higher levels of biological organization1,2,3. In such transitions, groups of individuals at one level (such as single cells) cooperate to form selective units at a higher level (such as multicellular organisms). Though the evolution of cooperation is difficult to observe directly in higher eukaryotes, microorganisms do offer such an opportunity4. Here we report the evolution of novel cooperative behaviour in experimental lineages of the bacterium Myxococcus xanthus. Wild-type strains of M. xanthus exhibit socially dependent swarming across soft surfaces5 by a mechanism known as ‘S-motility’ that requires the presence of extracellular type IV pili6. In lineages of M. xanthus unable to make pili, a new mechanistic basis for cooperative swarming evolved. Evolved swarming is mediated, at least in part, by enhanced production of an extracellular fibril matrix that binds cells—and their evolutionary interests—together. Though costly to individuals, fibril production greatly enhanced population expansion in groups of interconnected cells. These results show that fundamental transitions to primitive cooperation can readily occur in bacteria.

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Figure 1: Swarming rates and phenotypes of ancestral (A1, A2) and evolved (E1–E8) genotypes relative to WT on soft agar.
Figure 2: Swarming rates of WT, A1, A2, E7, E8, cglB and dsp mutants and LS1116 relative to WT on soft agar.
Figure 3
Figure 4: Evolution of fibril production.

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Acknowledgements

We are grateful to S. Bonhoeffer, S. Elena, L. Kroos, P. Rainey and W. Shi for discussion or comments, I. Dinkelacker and F. Fiegna for technical assistance, K. Hillesland for construction of strains A1 and A2, D. Kaiser and H. Kaplan for antibodies and plasmids, L. Shimkets for discussion and strains, and J. Berger and H. Schwarz for electron microscopy expertise and assistance.

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Authors and Affiliations

  1. Department of Evolutionary Biology, Max-Planck Institute for Developmental Biology, Spemannstrasse 35, 72076, Tübingen, Germany

    Gregory J. Velicer

  2. Department of Protein Evolution, Max-Planck Institute for Developmental Biology, Spemannstrasse 35, 72076, Tübingen, Germany

    Yuen-tsu N. Yu

Authors
  1. Gregory J. Velicer
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  2. Yuen-tsu N. Yu
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Correspondence to Gregory J. Velicer.

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Velicer, G., Yu, Yt. Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus. Nature 425, 75–78 (2003). https://doi.org/10.1038/nature01908

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