Social Interactions in Myxobacterial Swarming

Swarming, a collective motion of many thousands of cells, produces colonies that rapidly spread over surfaces. In this paper, we introduce a cell-based model to study how interactions between neighboring cells facilitate swarming. We chose to study Myxococcus xanthus, a species of myxobacteria, because it swarms rapidly and has well-defined cell–cell interactions mediated by type IV pili and by slime trails. The aim of this paper is to test whether the cell contact interactions, which are inherent in pili-based S motility and slime-based A motility, are sufficient to explain the observed expansion of wild-type swarms. The simulations yield a constant rate of swarm expansion, which has been observed experimentally. Also, the model is able to quantify the contributions of S motility and A motility to swarming. Some pathogenic bacteria spread over infected tissue by swarming. The model described here may shed some light on their colonization process.

[1]  Dale Kaiser,et al.  Bacterial Swarming: A Re-examination of Cell-Movement Patterns , 2007, Current Biology.

[2]  L. Emödy,et al.  The role of swarm cell differentiation and multicellular migration in the uropathogenicity of Proteus mirabilis. , 1994, The Journal of infectious diseases.

[3]  D. Kaiser,et al.  A three-dimensional model of myxobacterial aggregation by contact-mediated interactions. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Dale Kaiser,et al.  Cell movement and its coordination in swarms of myxococcus xanthus , 1983 .

[5]  George Oster,et al.  Breaking symmetry in myxobacteria , 2004, Current Biology.

[6]  James K Gimzewski,et al.  Nanoscale visualization and characterization of Myxococcus xanthus cells with atomic force microscopy. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Hong Sun,et al.  Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  W. Shi,et al.  Type IV Pilus-Dependent Motility and Its Possible Role in Bacterial Pathogenesis , 2002, Infection and Immunity.

[9]  M. Dworkin,et al.  Biochemical and structural analyses of the extracellular matrix fibrils of Myxococcus xanthus , 1994, Journal of bacteriology.

[10]  D. Zusman,et al.  Differential effects of chemoreceptor methylation‐domain mutations on swarming and development in the social bacterium Myxococcus xanthus , 2006, Molecular microbiology.

[11]  D. Kaiser,et al.  Type IV pili and cell motility , 1999, Molecular microbiology.

[12]  D. Zusman,et al.  "Frizzy" genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Vicsek,et al.  Novel type of phase transition in a system of self-driven particles. , 1995, Physical review letters.

[14]  M. Dworkin,et al.  Fibrils as extracellular appendages of bacteria: Their role in contact‐mediated cell‐cell interactions in Myxococcus xanthus , 1999, BioEssays : news and reviews in molecular, cellular and developmental biology.

[15]  R. Harshey,et al.  Bees aren't the only ones: swarming in Gram‐negative bacteria , 1994, Molecular microbiology.

[16]  Gerard T. Barkema,et al.  Monte Carlo Methods in Statistical Physics , 1999 .

[17]  Jonathan Hodgkin,et al.  Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): Two gene systems control movement , 2004, Molecular and General Genetics MGG.

[18]  D. Kaiser,et al.  Social gliding is correlated with the presence of pili in Myxococcus xanthus. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[19]  A. D. Kaiser,et al.  Gliding movements in Myxococcus xanthus , 1995, Journal of bacteriology.

[20]  Herbert Levine,et al.  Cooperative self-organization of microorganisms , 2000 .

[21]  Alex Mogilner,et al.  Two continuum models for the spreading of myxobacteria swarms , 2006, Bulletin of mathematical biology.

[22]  James K Gimzewski,et al.  Self-organized and highly ordered domain structures within swarms of Myxococcus xanthus. , 2006, Cell motility and the cytoskeleton.

[23]  L. Shimkets,et al.  Lipid chemotaxis and signal transduction in Myxococcus xanthus. , 2001, Trends in microbiology.

[24]  L. Jelsbak,et al.  The cell surface-associated intercellular C-signal induces behavioral changes in individual Myxococcus xanthus cells during fruiting body morphogenesis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[25]  W. Shi,et al.  Exopolysaccharide biosynthesis genes required for social motility in Myxococcus xanthus , 2004, Molecular microbiology.

[26]  Vicsek,et al.  Formation of complex bacterial colonies via self-generated vortices. , 1996, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[27]  Andreas Deutsch,et al.  Nonequilibrium clustering of self-propelled rods. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[28]  Dale Kaiser,et al.  Gliding motility and polarized slime secretion , 2007, Molecular microbiology.

[29]  Etienne Carbonnelle,et al.  A systematic genetic analysis in Neisseria meningitidis defines the Pil proteins required for assembly, functionality, stabilization and export of type IV pili , 2006, Molecular microbiology.

[30]  Howard C. Berg,et al.  Direct observation of extension and retraction of type IV pili , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Yi Jiang,et al.  CA Models of Myxobacteria Swarming , 2006, ACRI.

[32]  Roy D. Welch,et al.  Cell behavior in traveling wave patterns of myxobacteria , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Paul Singleton,et al.  Dictionary of Microbiology and Molecular Biology , 1993 .

[34]  Olga Sozinova,et al.  A three-dimensional model of myxobacterial fruiting-body formation , 2006, Proceedings of the National Academy of Sciences.

[35]  M. Dworkin,et al.  Integral proteins of the extracellular matrix fibrils of Myxococcus xanthus , 1994, Journal of bacteriology.

[36]  D. Helbing.  Traffic and related self-driven many-particle systems , 2000, cond-mat/0012229.

[37]  Dale Kaiser,et al.  Genetics of gliding motility in Myxococcus xanthus: Molecular cloning of the mgl locus , 1987, Molecular and General Genetics MGG.

[38]  Dale Kaiser,et al.  Coupling cell movement to multicellular development in myxobacteria , 2003, Nature Reviews Microbiology.

[39]  E. Hoiczyk,et al.  How Myxobacteria Glide , 2002, Current Biology.

[40]  M. Dworkin,et al.  Extracellular fibrils and contact-mediated cell interactions in Myxococcus xanthus , 1991, Journal of bacteriology.

[41]  D. Kaiser,et al.  Pulling Together with Type IV Pili , 2004, Journal of Molecular Microbiology and Biotechnology.

[42]  J. Mattick.  Type IV pili and twitching motility. , 2002, Annual review of microbiology.