The Library

Spatial simulations of myxobacterial development

Tools

Holmes, Antony, Kalvala, Sara and Whitworth, David E.. (2010) Spatial simulations of myxobacterial development. PLoS Computational Biology, Vol.6 (No.2). e1000686. ISSN 1553-734X

PDF
WRAP_Holmes_spacial_simulations.pdf - Draft Version - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader
Download (1214Kb)

Official URL: http://dx.doi.org/10.1371/journal.pcbi.1000686

Abstract

Understanding how relatively simple, single cell bacteria can communicate and coordinate their actions is important for explaining how complex multicellular behaviour can emerge without a central controller. Myxobacteria are particularly interesting in this respect because cells undergo multiple phases of coordinated behaviour during their life-cycle. One of the most fascinating and complex phases is the formation of fruiting bodies—large multicellular aggregates of cells formed in response to starvation. In this article we use evidence from the latest experimental data to construct a computational model explaining how cells can form fruiting bodies. Both in our model and in nature, cells move together in dense swarms, which collide to form aggregation centres. In particular, we show that it is possible for aggregates to form spontaneously where previous models require artificially induced aggregates to start the fruiting process.

Item Type:	Journal Article
Subjects:	Q Science > QR Microbiology
Divisions:	Faculty of Science > Molecular Organisation and Assembly in Cells (MOAC) Faculty of Science > Computer Science
Library of Congress Subject Headings (LCSH):	Myxobacterales -- Research, Bacteria -- Motility -- Mathematical models, Spatial analysis (Statistics), Monte Carlo method
Journal or Publication Title:	PLoS Computational Biology
Publisher:	Public Library of Science
ISSN:	1553-734X
Date:	26 February 2010
Volume:	Vol.6
Number:	No.2
Number of Pages:	13
Page Range:	e1000686
Identification Number:	10.1371/journal.pcbi.1000686
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	Engineering and Physical Sciences Research Council (EPSRC)
References:	1. Shapiro J (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52: 81–104. 2. McBride M (2001) Bacterial gliding motility: Multiple mechanisms for cell movement over surfaces. Annu Rev Microbiol 55: 49–75. 3. Wolgemuth C, Hoiczyk E, Kaiser D, Oster G (2002) How myxobacteria glide. Current Biology 12: 369–377. 4. Søgaard-Anderson L (2004) Cell polarity, intercellular signalling and morphogenetic cell movements in Myxococcus xanthus. Current Opinion in Microbiology 7: 587–593. 5. Kim S, Kaiser D (1991) C-factor has distinct aggregation and sporulation thresholds during Myxococcus development. Journal of Bacteriology 173: 1722–1728. 6. Kruse T, Lobedanz S, Berthelsen N, Søgaard-Anderson L (2001) C-signal: a cell surface-associated morphogen that induces and co-ordinates multicellular fruiting body morphogenesis and sporulation in Myxococcus xanthus. Molecular Microbiology 40: 156–168. 7. Kim S, Kaiser D (1990) C-factor: A cell-cell signaling protein required for fruiting body morphogenesis of M. Xanthus. Cell 61: 19–26. 8. Jelsbak L, Søgaard-Anderson L (2002) Pattern formation by a cell surfaceassociated morphogen in Myxococcus xanthus. Proc Natl Acad Sci USA 99: 2032–2037. 9. Jelsbak L, Søgaard-Anderson L (1999) The cell surface-associated intercellular csignal induces behavioral changes in individual Myxococcus xanthus cells during fruiting body morphogenesis. Proc Natl Acad Sci USA 96: 5031–5036. 10. Wu Y, Kaiser D, Alber M (2009) Periodic reversal of direction allows myxobacteria to swarm. Proc Natl Acad Sci USA 106: 1222–1227. 11. O’Connor K, Zusman D (1989) Patterns of cellular interactions during fruitingbody formation in Myxococcus xanthus. Journal of Bacteriology 171: 6013–6024. 12. White D (1984) Structure and function of myxobacteria cells and fruiting bodies. In: Rosenberg E, ed. Myxobacteria: Development and Cell Interactions, Springer-Verlag. pp 51–67. 13. Curtis P, Taylor R, Welch R, Shimkets L (2007) Spatial organization of Myxococcus xanthus during fruiting body formation. Journal of Bacteriology 189: 9126–9130. 14. White D (1993) Myxospore and fruiting body morphogenesis. In: Dworkin M, Kaiser D, eds. Myxobacteria II, American Society for Microbiology. pp 307–332. 15. Igoshin O, Welch R, Kaiser D, Oster G (2004) Waves and aggregation patterns in myxobacteria. Proc Natl Acad Sci USA 101: 4256–4261. 16. Grilione P, Pangborn J (1975) Scanning electron microscopy of fruiting body formation by myxobacteria. Journal of Bacteriology 124: 1558–1565. 17. Kuner J, Kaiser D (1982) Fruiting body morphogenesis in submerged cultures of Myxococcus xanthus. Journal of Bacteriology 151: 458–461. 18. Sozinova O, Jiang Y, Kaiser D, Alber M (2006) A three-dimensional model of myxobacterial fruiting-body formation. Proc Natl Acad Sci USA 103: 17255–17259. 19. Sozinova O, Jiang Y, Kaiser D, Alber M (2005) A three-dimensional model of myxobacterial aggregation by contact-mediated interactions. Proc Natl Acad Sci USA 102: 11308–11312. 20. Kaiser D, Welch R (2004) Dynamics of fruiting body morphogenesis. Journal of Bacteriology 186: 919–927. 21. Savill N, Hogeweg P (1996) Modelling morphogenesis: From single cells to crawling slugs. Journal of Theoretical Biology 184: 229–235. 22. Kaiser D (2003) Coupling cell movement to multicellular development in myxobacteria. Nature Reviews Microbiology 1: 45–54. 23. Zusman D, Scott A, Yang Z, Kirby J (2007) Chemosensory pathways, motility and development in Myxococcus xanthus. Nature Reviews Microbiology 5: 862–872. 24. Jelsbak L, Sogaard-Andersen L (2002) Pattern formation by a cell surfaceassociated morphogen in myxococcus xanthus. Proc Nat Acad Sciences, USA 99: 2032–2037. 25. Metropolis N, Rosenbluth A, Rosenbluth M, Teller A (1953) Equations of state calculations by fast computing machines. Journal of Chemical Physics 21: 1087–1092. 26. Glazier J, Graner F (1993) Simulation of the differential adhesion driven rearrangement of biological cells. Physical Review E 47: 2128–2154. 27. Potts R (1952) Some generalized order-disorder transformations. Mathematical Proceedings of the Cambridge Philosophical Society 48: 106–109. 28. Izaguirre J, Chaturvedi R, Huang C, Cickovski T, Coffland J, et al. (2003) Compucell, a multi-model framework for simulation of morphogenesis. Bioinformatics 20: 1129–1137. 29. Wu Y, Jiang Y, Kaiser D, Alber M (2007) Social interactions in myxobacterial swarming. PLoS Computational Biology 3: 2546–2558. 30. Pelling A, Li Y, Cross S, Castaneda S, Shi W, et al. (2006) Self-organized and highly ordered domain structures within swarms of Myxococcus xanthus, volume 63. Cell Motil Cytoskeleton. 31. Kaiser D, Dworkin M (2008) From glycerol to the genome. In: Whitworth D, ed. Myxobacteria: Multicellularity and Differentiation, ASM Press. pp 3–16. 32. Shimkets L, Dworkin M, Reichenbach H (2006) The myxobacteria. In: Dworkin M, ed. The Prokaryotes: a Handbook on the Biology of Bacteria, Springer, volume 7. pp 31–115. 33. Dworkin M (1996) Recent advances in the social and developmental biology of the Myxobacteria. Microbiological Reviews 60: 70–102. 34. Wireman JW, Dworkin M (1977) Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus. Journal of Bacteriology 129: 796–802. 35. Holmes A, Kalvala S, Whitworth D (2009) Myxobacteria motility: a novel 3D model of rippling behaviour in Myxococcus xanthus. Communications of the Systematics and Informatics World Network 6: 65–70. 36. Reichenbach H (1993) Biology of the myxobacteria: Ecology and taxonomy. In: Dworkin M, Kaiser D, eds. Myxobacteria II, American Society for Microbiology. pp 13–62. 37. Jelsbak L, Søgaard-Anderson L (2003) Cell behavior and cell-cell communication during fruiting body morphogenesis in Myxococcus xanthus. Journal of Microbiological Methods 55: 829–839. 38. Spormann A, Kaiser D (1995) Gliding movements in Myxococcus xanthus. Journal of Bacteriology 177: 5846–5852. 39. Starruss J, Bley T, Søgaard-Anderson L, Deutsch A (2007) A new mechanism for collective migration in Myxococcus xanthus. Journal of Statistical Physics 128: 269–286.
URI:	http://wrap.warwick.ac.uk/id/eprint/3015