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Understanding morphogenesis in myxobacteria from a theoretical and experimental perspective

By Antony Holmes

Abstract

Several species of bacteria exhibit multicellular behaviour, with individuals cells cooperatively working together within a colony. Often this has communal benefit since multiple cells acting in unison can accomplish far more than an individual cell can and the rewards can be shared by many cells. Myxobacteria are one of the most complex of the multicellular bacteria, exhibiting a number of different spatial phenotypes. Colonies engage in multiple emergent behaviours in response to starvation culminating in the formation of massive, multicellular fruiting bodies. \ud In this thesis, experimental work and theoretical modelling are used to investigate emergent behaviour in myxobacteria. Computational models were created using FABCell, an open source software modelling tool developed as part of the research to facilitate modelling large biological systems. \ud The research described here provides novel insights into emergent behaviour and suggests potential mechanisms for allowing myxobacterial cells to go from a vegetative state into a fruiting body. A differential equation model of the Frz signalling pathway, a key component in the regulation of cell motility, is developed. This is combined with a three-dimensional model describing the physical characteristics of cells using Monte Carlo methods, which allows thousands of cells to be simulated. The unified model explains how cells can ripple, stream, aggregate and form fruiting bodies. Importantly, the model copes with the transition between stages showing it is possible for the important myxobacteria control systems to adapt and display multiple behaviours

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OAI identifier: oai:wrap.warwick.ac.uk:2758

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  1. (2004). A biochemical oscillator explains several aspects of Myxococcus xanthus behavior during development. doi
  2. (2007). A course in ordinary differential equations. Chapman and Hall/CRC,
  3. (2005). A framework for threedimensional simulation of morphogenesis. doi
  4. (2006). A generalised discrete model linking rippling pattern formation and individual cell reversal statistics in colonies of myxobacteria. doi
  5. A model for individual and collective cell movement in Dictyostelium discoideum. doi
  6. (2004). A multi-algorithm, multitimescale method for cell simulation. doi
  7. (2002). A new kind of science, chapter 2: The crucial experiment.
  8. (2007). A new mechanism for collective migration in Myxococcus xanthus. doi
  9. (2000). A stochastic cellular automaton modelling gliding and aggregation of myxobacteria. doi
  10. (2005). A three-dimensional model of myxobacterial aggregation by contact-mediated interactions. doi
  11. (2006). A three-dimensional model of myxobacterial fruiting-body formation. doi
  12. (2006). Accordion waves in Myxococcus xanthus. doi
  13. (2005). Agentcell: a digital single-cell assay for bacterial chemotaxis. doi
  14. (2007). Aggregation during fruiting body formation in Myxococcus xanthus is driven by reducing cell movement. doi
  15. (2009). AglZ regulates adventurous (A-) motility in emphMyxococcus xanthus through its interaction with the cytoplasmic receptor, doi
  16. (2005). An individual based model of rippling movement in a myxobacteria population. doi
  17. (2004). Analysis of the frz signal transduction system of Myxococcus xanthus shows the importance of the conserved C-terminal region of the cytoplasmic chemoreceptor FrzCD in sensing signals. doi
  18. (1984). Antibiotics and lytic enzymes. doi
  19. (2009). Argonne National Laboratory. Repast agent simulation toolkit. http://repast.sourceforge.net/,
  20. (1991). Behavior of peripheral rods and their role in the life cycle of Myxococcus xanthus.
  21. (2006). Biological evaluation of tubulysin a: a potential anticancer and antiangiogenic natural product. doi
  22. (2004). Biological lattice gas models. doi
  23. (1993). Biology of the myxobacteria: ecology and taxonomy. doi
  24. (2006). Bioremediation of weathered-building stone surfaces. doi
  25. (2004). Breaking symmetry in myxobacteria. doi
  26. C factor, a cell-surface-associated intercellular signaling protein, stimulates the cytoplasmic Frz signal transduction system in Myxococcus xanthus. doi
  27. (1991). C-factor has distinct aggregation and sporulation thresholds during Myxococcus development.
  28. (1990). C-factor: A cell-cell signaling protein required for fruiting body morphogenesis doi
  29. (2001). C-signal: a cell surface-associated morphogen that induces and co-ordinates multicellular fruiting body morphogenesis and sporulation in Myxococcus xanthus. doi
  30. (2008). C# 3.0 design patterns, chapter 1: C# meets design patterns. O’Reilly,
  31. (2008). C# 3.0 design patterns, chapter 10: Behavioral patterns: visitor, interpreter, and memento. O’Reilly,
  32. (2008). C# 3.0 design patterns, chapter 2: structural patterns: decorator, proxy, bridge. O’Reilly,
  33. (2002). C++: the complete reference, fourth edition.
  34. (2008). CA models of myxobacterial swarming. doi
  35. (1990). Cell alignment required in differentiation of Myxococcus xanthus. doi
  36. (2003). Cell behavior and cell-cell communication during fruiting body morphogenesis in Myxococcus xanthus. doi
  37. (2001). Cell behavior in traveling wave patterns of myxobacteria. doi
  38. (1996). Cell density regulates cellular reversal frequency in Myxococcus xanthus. doi
  39. (1977). Cell density-dependent growth of Myxococcus xanthus on casein.
  40. (2004). Cell polarity, intercellular signalling and morphogenetic cell movements in Myxococcus xanthus. doi
  41. (1988). Cell surface properties correlated with cohesion in Myxococcus xanthus.
  42. (2005). Cellular automaton: modelling of biological pattern formation. Birkhauser, doi
  43. (2004). chapter The Isling model and the Metropolis algorithm.
  44. (2008). chapter5: creationalpatterns: prototypes, factory method and singleton. O’Reilly,
  45. (2008). chapter9: BehavioralPatterns: iterator, mediator, and observer. O’Reilly,
  46. Chemosensory pathways, motility and development doi
  47. (1989). Communication and Concurrency.
  48. (1968). Comparative intermediary metabolism of vegetative cells and microcysts of Myxococcus xanthus.
  49. (2003). Competitive fates of bacterial social parasites: persistence and self-induced extinction of Myxococcus xanthus cheaters. The Royal Society, doi
  50. (2003). Compucell, a multi-model framework for simulation of morphogenesis. doi
  51. (2002). Computational challenges in cell simulation: a software engineering approach. doi
  52. (2003). Conservation of ornamental stone by Myxococcus xanthusinduced carbonate biomineralization. doi
  53. (2000). Construction of a genetic toggle switch in Escherichia coli.
  54. (1965). Cooperating sequential processes. doi
  55. (2007). Coupling of protein localization and cell movements by a dynamically localized response regulator in Myxococcus xanthus. doi
  56. (2005). Cross talking of network motifs in gene regulation that generates temporal pulses and spatial stripes. doi
  57. (1990). CsgA, an extracellular protein essential for Myxcoccus xanthus development.
  58. (2004). Detection of multistability, bifurcations, and hysteresis in a large class of biological positive-feedback systems. doi
  59. (1991). Development in Myxococcus xanthus involves differentiation into two cell types, peripheral rods and spores.
  60. (1962). Developmental biology of Myxococcus. doi
  61. (1990). Developmental sensory transduction in Myxococcus xanthus involves methylation and demethylation of FrzCD.
  62. (1977). Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus. doi
  63. Discovery and development of the epothilones : a novel class of antineoplastic drugs. doi
  64. (2005). Distributed cell biology simulations with E-Cell system. doi
  65. (1999). E-Cell: software environment for whole cell simulation. doi
  66. (2002). Engineered gene circuits. doi
  67. (1953). Equations of state calculations by fast computing machines. doi
  68. (2007). Evidence that focal adhesion complexes power bacterial gliding motility. doi
  69. (2006). Evolution of sensory complexity recorded in a myxobacterial genome. doi
  70. (1962). Fine structures of Myxococcus xanthus during morphogenesis. doi
  71. (2005). Force and flexibility of flailing myxobacteria. doi
  72. (1985). Frizzy genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility. doi
  73. Frizzy’ mutants: a new class of aggregation-defective developmental mutants of Myxococcus xanthus.
  74. (2008). From glycerol to the genome. doi
  75. (1982). Fruiting body morphogenesis in submerged cultures of Myxococcus xanthus.
  76. (1975). Fruiting-body formation and myxospore differentiation and germination in Myxococcus xanthus viewed by scanning electron microscopy.
  77. FrzCD, a methyl-accepting taxis protein from Myxococcus xanthus, shows modulated methylation during fruiting body formation.
  78. Further observations on the myxobacteriaceae. doi
  79. (2008). Genetic circuitry controlling motility behaviors of Myxococcus xanthus. doi
  80. (1979). Genetics of gliding motility in Myxococcus xanthus (myxobacterales): Two gene systems control movement. doi
  81. (1999). Gliding motility in bacteria: Insights from studies of Myxococcus xanthus.
  82. (1995). Gliding movements in Myxococcus xanthus. doi
  83. (1999). Gliding mutants of Myxococcus xanthus with high reversal frequencies and small displacements.
  84. (2001). Glycerol 3-phosphate inhibits swarming and aggregation of Myxococcus xanthus. doi
  85. (1980). Guanosine pentaphosphate and guanosine tetraphosphate accumulation and induction of myxococcus xanthus fruiting body development.
  86. (1975). Guarded commands, non-determinacy and formal derivation of programs. doi
  87. (1993). How and why bacteria talk to each other. doi
  88. (2002). How myxobacteria glide. doi
  89. (1988). Identification and characterization of the Myxococcus xanthus bsgA gene product. doi
  90. (1982). Induction of coordinated movement of Myxococcus xanthus cells.
  91. Induction of morphogenesis by methionine starvation in Myxococcus xanthus: polyamine control.
  92. (2008). Initiation and early developmental events. doi
  93. (2005). Inorganic polyphosphate in the social life of Myxococcus xanthus: Motility, development, and predation. doi
  94. (1994). Intercellular C-signaling and the traveling waves of Myxococcus. doi
  95. (1993). Intercellular signaling. doi
  96. (1999). Intercellularsignalingduringfruiting-bodydevelopmentofMyxococcus xanthus.
  97. (2008). Introduction to differential equations with dynamical systems.
  98. (1998). Isolation of myxobacteria from the marine environment.
  99. (2007). J.Weyers, andA.Jones. Practicalskillsinbiomolecularsciences, third edition.
  100. (2009). Jade (java agent development framework). http://jade.cselt.it/,
  101. (2009). Java vs. c++. http://verify.stanford.edu/uli/java_cpp.html,
  102. (2003). Lattice gas cellular automation model for rippling and aggregation in myxobacteria. Physica D, doi
  103. (2009). Localization of a bacterial cytoplasmic receptor is dynamic and changes with cell-cell contacts. doi
  104. Making waves: pattern formation by a cell-surface-associated signal. doi
  105. (2004). MASON: a new multi-agent simulation toolkit.
  106. (1970). Mathematical games: The fantastic combinations of John Conway’s new solitaire game ”life”.
  107. (1990). Methods and logics for proving programs. doi
  108. (2009). MiKTeX project page. http://miktex.org/,
  109. (1996). Modeling biological systems: principles and applications, chapter 1: Uses of scientific models.
  110. (1996). Modeling biological systems: principles and applications, chapter 2: the modeling process. Chapman and Hall, doi
  111. (1996). Modelling morphogenesis: from single cells to crawling slugs. doi
  112. (2004). Monte Carlo methods in statistical physics. doi
  113. (2003). Multiagent systems for the simulation of land-use and land-cover change: a review. doi
  114. (2007). Multicellular development in Myxococcus xanthus is stimulated by predator-prey interactions. doi
  115. (2001). multiplemechanismsforcellmovement over surfaces.
  116. (2005). Mutations affecting predation ability of the soil bacterium Myxococcus xanthus. doi
  117. (2009). Myxobacteria motility: a novel 3D model of rippling behaviour in Myxococcus xanthus.
  118. (1984). Myxobacteria: a most peculiar group of social prokaryotes. doi
  119. Myxobacteria: cell interactions, genetics and development. doi
  120. (1984). Myxobacteria: development and cell interactions. doi
  121. (1993). Myxococcus xanthus encodes an ATPdependent protease which is required for developmental gene transcription and intercellular signaling.
  122. (1993). Myxospore and fruiting body morphogenesis.
  123. (2006). Novel lipids in Myxococcus xanthus and their role in chemotaxis. doi
  124. (1990). Nucleotide sequence and transcriptional products of the csg locus of Myxococcus xanthus.
  125. (1978). Nutrition of Myxococcus xanthus, a fruiting myxobacterium. doi
  126. (1962). Nutritional requirements for vegetative growth of Myxococcus xanthus.
  127. (2000). On agent-based software engineering. doi
  128. (2003). On cellular automaton approaches to modeling biological cells. doi
  129. (2009). OpenOffice.org: the free and open productivity suite. http://www.openoffice.org/, doi
  130. (2001). Pattern formation and traveling waves in myxobacteria: theory and modeling. doi
  131. Pattern formation by a cell surfaceassociated morphogen in Myxococcus xanthus. doi
  132. (1989). Patterns of cellular interactions during fruiting-body formation in Myxococcus xanthus. doi
  133. (2009). Periodic reversal of direction allows myxobacteria to swarm. doi
  134. (2009). Persistence of Vision Raytracer Pty. Ltd. POV-Ray: the persistence of vision raytracer. http://www.povray.org/,
  135. (2008). Phosphate acquisition components of the Myxococcus xanthus Pho regulon are regulated by both phosphate availability and development. doi
  136. (1998). Pitfalls of agent-oriented development. doi
  137. (2009). Posix threads programming. https://computing.llnl.gov/tutorials/pthreads/,
  138. (2003). Practical object-oriented design with UML, second edition.
  139. (2008). Predataxis behavior in Myxococcus xanthus. doi
  140. (2004). Programmable cells: Interfacing natural and engineered gene networks. doi
  141. (1996). Recent advances in the social and developmental biology of the Myxobacteria.
  142. (2005). Regulated pole-to-pole oscillations of a bacterial gliding motility protein. doi
  143. (1975). Regulation of development in Myxococcus xanthus: effect of 3’:5’-cyclic AMP, ADP, and nutrition. doi
  144. (2008). Reversing cells and oscillating motility proteins. doi
  145. (2008). Reversing Myxococcus xanthus polarity. doi
  146. (2006). Rippling is a predatory behavior in Myxococcus xanthus. doi
  147. Rippling of myxobacteria. doi
  148. (2002). Rippling patterns in aggregates of myxobacteria arise from cell-cell collisions. Physical Review, doi
  149. (1993). Roland Thaxter’s legacy and the origins of multicellular development.
  150. (2004). Role of streams in myxobacteria aggregate formation. doi
  151. (1975). Scanning electron microscopy of fruiting body formation by myxobacteria.
  152. (2006). Selforganized and highly ordered domain structures within swarms of Myxococcus xanthus, volume 63. Cell Motil. Cytoskeleton, doi
  153. (2002). Short protocols in molecular biology, fifth edition. doi
  154. (2004). Signaling in myxobacteria. doi
  155. (2004). Signaling switches and bistability arising from multisite phosphorylation in protein kinase cascades. doi
  156. Simulation of biological cell sorting using a twodimensional extended potts model. doi
  157. (1993). Simulation of the differential adhesion driven rearrangement of biological cells. Physical Review E, doi
  158. (1979). Social gliding is correlated with the presence of pili in Myxococcus xanthus. doi
  159. (2007). Social interactions in myxobacterial swarming. doi
  160. (1999). Software engineering with agents: pitfalls and pratfalls. doi
  161. (2004). Software engineering, seventh edition, chapter 23: Software testing.
  162. (2004). Software engineering, seventh edition.
  163. (2009). Software Foundation. Gnu scientific library. http://www.gnu.org/software/gsl/,
  164. (2009). Software Foundation. The gnu compiler collection. http://gcc.gnu.org/,
  165. (2008). Sofware Engineering: principles and practice, third edition, chapter 13: Software testing. John Wiley and Sons,
  166. (2008). Sofware Engineering: principles and practice, third edition, chapter 15: software tools.
  167. (2008). Sofware Engineering: principles and practice, third edition, chapter 9: requirements engineering.
  168. (2008). Sofware Engineering: principles and practice, third edition.
  169. (1952). Some generalized order-disorder transformations. doi
  170. (2007). Spatial organization of Myxococcus xanthus during fruiting body formation. doi
  171. (2004). Strategies of microbial cheater control. doi
  172. (1969). Structural changes in Stigmatella aurantiaca during myxospore induction.
  173. (1984). Structure and function of myxobacteria cells and fruiting bodies. doi
  174. (2009). SwarmWiki: tools for agent-based modelling. http://www.swarm.org/,
  175. (2009). Systems biology markup language. http://sbml.org/, doi
  176. (1987). The beginning of the Monte Carlo method.
  177. (1999). The cell surface-associated intercellular csignal induces behavioral changes in individual Myxococcus xanthus cells during fruiting body morphogenesis. doi
  178. (2009). The CellML project. The cellml project. http://www.cellml.org/, doi
  179. (2008). The dynamics of myxobacteria life cycle.
  180. (2007). The elusive engine in Myxococcus xanthus gliding motility. doi
  181. (2006). The essentials of computer organization and architecture, second edition. Jones and Bartlett Publishers,
  182. (1966). The fate of the cell envelopes of Myxococcus xanthus during microcyst germination. doi
  183. (2006). The myxobacteria. doi
  184. (2009). The Open MPI Project. Open MPI: open source high performance computing. http://www.open-mpi.org/, doi
  185. (1982). The Potts model. doi
  186. (1993). The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces. doi
  187. The twocomponent signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. doi
  188. (1966). Theory of self-reproducing automata. doi
  189. (1998). Thinking about bacterial populations as multicellular organisms. doi
  190. (1995). Trail following and aggregation of myxobacteria. doi
  191. (1982). Trail following by gliding bacteria.
  192. (2007). Two localization motifs mediate polar residence of frzs during cell movement and reversals of Myxococcus xanthus. doi
  193. (2004). Two-stage aggregate formation via streams in myxobacteria. doi
  194. (1995). Understanding the Metropolis-Hastings algorithm. doi
  195. Use of a phase variation-specific promoter of Myxococcus xanthus in a strategy for isolating a phase-locked mutant.
  196. (2004). Waves and aggregation patterns in myxobacteria. doi
  197. (2004). XML in a nutshell, third edition, chapter 1: XML concepts. O’Reilly,

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