Physical schemata underlying biological pattern formation—examples, issues and strategies

Levine, Herbert; Ben‐Jacob, Eshel

doi:10.1088/1478-3967/1/2/p01

Cited by 49 publications

(43 citation statements)

References 24 publications

(21 reference statements)

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“…Common features displayed by these self-organized phenomena are the formation of trails that lead to the emergence of dramatic patterns of large-scale order (15). The processes leading to pattern formation in biological systems are likely to be more complex than the spontaneous emergence of patterns that are observed in nonliving systems and will involve an interplay of physical, chemical, and biological parameters (16,17).…”

mentioning

confidence: 99%

Self-organization of bacterial biofilms is facilitated by extracellular DNA

Gloag¹,

Turnbull²,

Huang

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

253

269

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Twitching motility-mediated biofilm expansion is a complex, multicellular behavior that enables the active colonization of surfaces by many species of bacteria. In this study we have explored the emergence of intricate network patterns of interconnected trails that form in actively expanding biofilms of Pseudomonas aeruginosa. We have used high-resolution, phase-contrast time-lapse microscopy and developed sophisticated computer vision algorithms to track and analyze individual cell movements during expansion of P. aeruginosa biofilms. We have also used atomic force microscopy to examine the topography of the substrate underneath the expanding biofilm. Our analyses reveal that at the leading edge of the biofilm, highly coherent groups of bacteria migrate across the surface of the semisolid media and in doing so create furrows along which following cells preferentially migrate. This leads to the emergence of a network of trails that guide mass transit toward the leading edges of the biofilm. We have also determined that extracellular DNA (eDNA) facilitates efficient traffic flow throughout the furrow network by maintaining coherent cell alignments, thereby avoiding traffic jams and ensuring an efficient supply of cells to the migrating front. Our analyses reveal that eDNA also coordinates the movements of cells in the leading edge vanguard rafts and is required for the assembly of cells into the "bulldozer" aggregates that forge the interconnecting furrows. Our observations have revealed that large-scale self-organization of cells in actively expanding biofilms of P. aeruginosa occurs through construction of an intricate network of furrows that is facilitated by eDNA.collective behavior | t4p | type IV pili | tfp | swarming

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mentioning

confidence: 99%

Self-organization of bacterial biofilms is facilitated by extracellular DNA

Gloag¹,

Turnbull²,

Huang

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

253

269

View full text Add to dashboard Cite

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“…It has been suggested that there may be significant benefit in such collective community-level behavior and that such organism aggregations behave with a remarkable degree of plasticity and adaptability that allows them enhanced capability to meet changing and challenging growth conditions [20]. Obviously such plasticity with respect to the environment would be particularly pertinent to extremophile organisms living in an array of especially challenging physical and chemical conditions.…”

Section: Extremophilesmentioning

confidence: 99%

Estimation, Modeling, and Simulation of Patterned Growth in Extreme Environments

Strader¹,

Schubert

Quintana³

et al. 2011

Advances in Experimental Medicine and Biology

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In the search for life on Mars and other extraterrestrial bodies or in our attempts to identify biological traces in the most ancient rock record of Earth, one of the biggest problems facing us is how to recognize life or the remains of ancient life in a context very different from our planet's modern biological examples. Specific chemistries or biological properties may well be inapplicable to extraterrestrial conditions or ancient Earth environments. Thus, we need to develop an arsenal of techniques that are of broader applicability. The notion of patterning created in some fashion by biological processes and properties may provide such a generalized property of biological systems no matter what the incidentals of chemistry or environmental conditions. One approach to recognizing these kinds of patterns is to look at apparently organized arrangements created and left by life in extreme environments here on Earth, especially at various spatial scales, different geologies, and biogeochemical circumstances.

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“…Materials exhibiting such properties (though not typically all at once) also exist outside biology, where they are known as 'soft matter' [6] and 'excitable media' [7,8].…”

Section: Introductionmentioning

confidence: 99%

‘Biogeneric’ developmental processes: drivers of major transitions in animal evolution

Newman

2016

Phil. Trans. R. Soc. B

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One contribution of 13 to a theme issue 'The major synthetic evolutionary transitions'. Using three examples drawn from animal systems, I advance the hypothesis that major transitions in multicellular evolution often involved the constitution of new cell-based materials with unprecedented morphogenetic capabilities. I term the materials and formative processes that arise when highly evolved cells are incorporated into mesoscale matter 'biogeneric', to reflect their commonality with, and distinctiveness from, the organizational properties of non-living materials. The first transition arose by the innovation of classical cell-adhesive cadherins with transmembrane linkage to the cytoskeleton and the appearance of the morphogen Wnt, transforming some ancestral unicellular holozoans into 'liquid tissues', and thereby originating the metazoans. The second transition involved the new capabilities, within a basal metazoan population, of producing a mechanically stable basal lamina, and of planar cell polarization. This gave rise to the eumetazoans, initially diploblastic (twolayered) forms, and then with the addition of extracellular matrices promoting epithelial-mesenchymal transformation, three-layered triploblasts. The last example is the fin-to-limb transition. Here, the components of a molecular network that promoted the development of species-idiosyncratic endoskeletal elements in gnathostome ancestors are proposed to have evolved to a dynamical regime in which they constituted a Turing-type reaction-diffusion system capable of organizing the stereotypical arrays of elements of lobe-finned fish and tetrapods. The contrasting implications of the biogeneric materialsbased and neo-Darwinian perspectives for understanding major evolutionary transitions are discussed.This article is part of the themed issue 'The major synthetic evolutionary transitions'.

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Physical schemata underlying biological pattern formation—examples, issues and strategies

Cited by 49 publications

References 24 publications

Self-organization of bacterial biofilms is facilitated by extracellular DNA

Self-organization of bacterial biofilms is facilitated by extracellular DNA

Estimation, Modeling, and Simulation of Patterned Growth in Extreme Environments

‘Biogeneric’ developmental processes: drivers of major transitions in animal evolution

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