What do colony patterns mean? - A biologist’s view James A. Shapiro, University of Chicago 1. The colony as an organized, differentiated structure with a complex morphogenesis, even laboratory E. coli. 2. Patterns that reflect the formation of adaptive structures: genetic analysis. 3. A pattern that reflects the operation of adaptive systems under defined conditions: environmental analysis and modeling (Proteus mirabilis). 4. The dense-branching morphology of B. subtilis colonies under nutritional restriction: a problem for modeling.

Clonal and Non-clonal Patterns in E. coli Colonies

Initiation of E. coli colony development

Morphogenesis and cellular differentiation in E. coli

Colony differentiation into organized regions: E. coli

Patterns that reflect the formation of adaptive structures: E. coli Budrene EO, Berg HC. Dynamics of formation of symmetrical patterns by chemotactic bacteria. Nature (6535):

Patterns that reflect the formation of adaptive structures: B. subtilis Fruiting Body Formation by Bacillus subtilis Steven S. Branda 1†, José Eduardo González-Pastor 2†, Sigal Ben-Yehuda 2, Richard Losick 2 and Roberto Kolter. Proc. Nat. Acad. Sci. USA, 98:

Patterns that reflect the formation of adaptive structures: genetic analysis Esteban Lombardía, Adrián J. Rovetto, Ana L. Arabolaza, and Roberto R. Grau. A LuxS-Dependent Cell-to- Cell Language Regulates Social Behavior and Development in Bacillus subtilis. Journal of Bacteriology, June 2006, p , Vol. 188

A pattern that reflects the operation of adaptive systems under defined conditions: Proteus mirabilis. Where modeling matters most. Synchronous inoculationAsynchronous inoculation (1 hr)

Proteus Crew L-R: Todd Dupont, Mitsugu Matsushita, Bruce Ayati, Oliver Rauprich, JAS, Sergei Esipov & Sune Danø

Different cell types in Proteus swarming

Distinct roles of glucose and amino acids in growth and swarming

Dependence of swarming velocity on amino acid, not glucose concentration (above a threshold) Sune Danø

Robust Periodicity in Proteus Swarming Rauprich O, Matsushita M, Weijer K, Siegert F, Esipov S, Shapiro JA Periodic phenomena in Proteus mirabilis swarm colony development. J. Bacteriol. 178:

Independence of swarm period from swarming velocity (amino acids) Sune Danø

Interlocking Cell Cycles Esipov, S. and J.A.Shapiro Kinetic model of Proteus mirabilis swarm colony development. J. Math. Biol. 36,

Kinetic Equations Esipov, S. and J.A.Shapiro Kinetic model of Proteus mirabilis swarm colony development. J. Math. Biol. 36, Diffusivity Spatially Resolved Kinetics Swarmer cell density

Robust periodicity requires age- dependent dedifferentiation Bruce P. Ayati. Modeling the role of the cell cycle in regulating Proteus mirabilis swarm-colony development. Applied Mathematics Letters 20 (2007) 913–918

Experimental examination of Proteus dedifferentiation A. Liew & JAS

The dense-branching morphology of B. subtilis colonies under nutritional restriction: a problem ripe for modeling. Fujikawa H, and Matsushita M Fractal growth of Bacillus subtilis on agar plates. J. Phys. Soc. Japan 58:

Amino acid-dependent branching at different temperatures Julkowska DJulkowska D, Obuchowski M, Holland IB, Séror SJ Branched swarming patterns on a synthetic medium formed by wild-type Bacillus subtilis strain 3610: detection of different cellular morphologies and constellations of cells as the complex architecture develops. Microbiology 150: Obuchowski MHolland IBSéror SJ

Motility occurs in a small “fingernail” region at the tip of each dendrite M. Matsushita

Observations and hypotheses for modeling B. subtilis DBM Observations: 1.Amino acids necessary (I.B. Holland, personal communication) 2.DBM limited to a special region of the nutritional-mobility space 3.DBM characterized by branches that do not grow in width 4.Tip-splitting occurs when branches separated by a critical distance 5.Increased cell activity in a limited zone at the tip of each dendrite Hypotheses: 1.Tip expansion requires active cell movement inside front 2.Cell movement occurs only above a threshold amino acid level 3.Cell movement is the major sink for amino acid consumption 4.Glucose-based growth is not nutritionally limited