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

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Initiation of E. coli colony development

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Morphogenesis and cellular differentiation in E. coli

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Colony differentiation into organized regions: E. coli

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Patterns that reflect

the formation of

adaptive structures:

E. coli

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are needed to see this picture.Budrene EO, Berg HC. Dynamics of formation of symmetrical patterns by chemotactic bacteria.Nature. 1995 376(6535):49-53.

Patterns that reflect the formation of adaptive structures: B. subtilis

Fruiting Body Formation by Bacillus subtilis Steven S. Branda1†, José Eduardo González-Pastor2†, Sigal Ben-Yehuda2, Richard Losick2 and Roberto Kolter. Proc. Nat. Acad. Sci. USA, 98: 11621-11626

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. 4442-4452, Vol. 188

A pattern that reflects the operation of adaptive systems under defined conditions: Proteus mirabilis. Where modeling matters most.

Synchronous inoculation Asynchronous inoculation (1 hr)

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

Different cell types in Proteus

swarming

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Distinct roles of glucose and amino acids in growth and swarming

Dependence of swarming velocity on amino acid, not glucose concentration

(above a threshold)

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Sune Danø

Robust Periodicity in Proteus Swarming

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Hours at 32 C

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Lag 1st swarm 1st consol. 2nd swarm 2nd consol.

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Lag 1st swarm 1st consol. 2nd swarm 2nd consol.

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Rauprich O, Matsushita M, Weijer K, Siegert F, Esipov S, Shapiro JA. 1996. Periodic phenomena in Proteus mirabilis swarm colony development. J. Bacteriol. 178:6525-38

Independence of swarm period from swarming velocity (amino acids)

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Sune Danø

Interlocking Cell Cycles

τd

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Esipov, S. and J.A.Shapiro. 1998. Kinetic model of Proteus mirabilis swarm colony development. J. Math. Biol. 36, 249-268.

Kinetic Equations

Esipov, S. and J.A.Shapiro. 1998. Kinetic model of Proteus mirabilis swarm colony development. J. Math. Biol. 36, 249-268.

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. 1989. Fractal growth of Bacillus subtilis on agar plates. J. Phys. Soc. Japan 58:3875-78

Amino acid-dependent branching at different temperatures

Julkowska D, Obuchowski M, Holland IB, Séror SJ. 2004. 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 150:1839-49.

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 space3. DBM characterized by branches that do not grow in width4. Tip-splitting occurs when branches separated by a critical distance5. Increased cell activity in a limited zone at the tip of each dendrite

Hypotheses:1. Tip expansion requires active cell movement inside front2. Cell movement occurs only above a threshold amino acid level3. Cell movement is the major sink for amino acid consumption4. Glucose-based growth is not nutritionally limited