Chemotactic smoothing of collective migration

Bhattacharjee, Tapomoy; Amchin, Daniel B.; Alert, Ricard; Ott, Jenna; Datta, Sujit S.

doi:10.7554/elife.71226

Cited by 36 publications

(50 citation statements)

References 102 publications

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“…It was recently shown that colonies of motile E. coli in similar matrices but with larger pores—sufficiently large for cells to swim through—smooth out any perturbations to their colony morphology using directed motility, retaining flat, cylindrical surfaces [35, 36]. We observe starkly-differing behavior for the case of purely growth-driven colony expansion considered here.…”

Section: Resultsmentioning

confidence: 65%

“…Our experiments used five different bacterial strains: E. coli W3110 (motile) and ΔflhDC (non-motile), both of which constitutively express GFP; V. cholerae JY030 [148]; P. aeruginosa PAO 1 ΔfliC; and K. sucrofermentans ATCC-700178. In each experiment, we first prepare a dense suspension of cells in the liquid cell culture medium used to swell the granular hydrogel matrix, and then use this suspension as the inoculum that is 3D-printed into the matrix, following our previous work [34, 35].…”

Section: Methodsmentioning

confidence: 99%

“…Preparing hydrogel matrices.The 3D granular hydrogel matrices are prepared following our prior work [34,35] by dispersing dry granules of crosslinked acrylic acid/alkyl acrylate copolymers (Carbomer 980, Ashland or Carbopol 980NF, Lubrizol) in liquid cell culture media.…”

Section: Methodsmentioning

confidence: 99%

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Roughening instability of growing 3D bacterial colonies

Martínez-Calvo

Bhattacharjee

Bay

et al. 2022

Preprint

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How do growing bacterial colonies get their shapes? While colony morphogenesis is well-studied in 2D, many bacteria grow as large colonies in 3D environments, such as gels and tissues in the body, or soils, sediments, and subsurface porous media. Here, we describe a morphological instability exhibited by large colonies of bacteria growing in 3D. Using experiments in transparent 3D granular hydrogel matrices, we show that dense colonies of four different species of bacteria—Escherichia coli, Vibrio cholerae, Pseudomonas aeruginosa, and Komagataeibacter sucrofermentans—generically roughen as they consume nutrients and grow beyond a critical size, eventually adopting a characteristic branched, broccoli-like, self-affine morphology independent of variations in the cell type and environmental conditions. This behavior reflects a key difference between 2D and 3D colonies: while a 2D colony may access the nutrients needed for growth from the third dimension, a 3D colony inevitably becomes nutrient-limited in its interior, driving a transition to rough growth at its surface. We elucidate the onset of roughening using linear stability analysis and numerical simulations of a continuum model that treats the colony as an ‘active fluid’ whose dynamics are driven by nutrient-dependent cellular growth. We find that when all dimensions of the growing colony substantially exceed the nutrient penetration length, nutrient-limited growth drives a 3D morphological instability that recapitulates essential features of the experimental observations. Our work thus provides a framework to predict and control the organization of growing colonies—as well as other forms of growing active matter, such as tumors and engineered living materials—in 3D environments.

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Section: Resultsmentioning

confidence: 65%

Section: Methodsmentioning

confidence: 99%

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Roughening instability of growing 3D bacterial colonies

Martínez-Calvo

Bhattacharjee

Bay

et al. 2022

Preprint

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“…Moreover, because our model describes spreading over large length and time scales, we expect it could help more accurately describe the spreading dynamics of bacteria in processes ranging from infections, drug delivery, agriculture, and bioremediation. To this end, it would be interesting to extend our one-dimensional simulations to higher dimensions, which could result in additional rich dynamics e.g., as recently explored in [ 73 ], and to media with spatially-varying confinement.…”

Section: Discussionmentioning

confidence: 99%

Influence of confinement on the spreading of bacterial populations

et al. 2022

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The spreading of bacterial populations is central to processes in agriculture, the environment, and medicine. However, existing models of spreading typically focus on cells in unconfined settings—despite the fact that many bacteria inhabit complex and crowded environments, such as soils, sediments, and biological tissues/gels, in which solid obstacles confine the cells and thereby strongly regulate population spreading. Here, we develop an extended version of the classic Keller-Segel model of bacterial spreading via motility that also incorporates cellular growth and division, and explicitly considers the influence of confinement in promoting both cell-solid and cell-cell collisions. Numerical simulations of this extended model demonstrate how confinement fundamentally alters the dynamics and morphology of spreading bacterial populations, in good agreement with recent experimental results. In particular, with increasing confinement, we find that cell-cell collisions increasingly hinder the initial formation and the long-time propagation speed of chemotactic pulses. Moreover, also with increasing confinement, we find that cellular growth and division plays an increasingly dominant role in driving population spreading—eventually leading to a transition from chemotactic spreading to growth-driven spreading via a slower, jammed front. This work thus provides a theoretical foundation for further investigations of the influence of confinement on bacterial spreading. More broadly, these results help to provide a framework to predict and control the dynamics of bacterial populations in complex and crowded environments.

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“…Other work studying E. coli in 3D environments has shown that chemotaxis enables large-scale perturbations to the overall morphology of a population to be smoothed out as cells migrate, enabling them to continue to migrate together as a coherent band 252 . This population-scale smoothing unexpectedly reflects the manner in which individual cells transduce external signals during chemotaxis.…”

Section: External Stimulimentioning

confidence: 99%

Active transport in complex environments

Martínez-Calvo¹,

Trenado-Yuste²,

Datta³

2021

Preprint

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The ability of many living systems to actively self-propel underlies critical biomedical, environmental, and industrial processes. While such active transport is well-studied in uniform settings, environmental complexities such as geometric constraints, mechanical cues, and external stimuli such as chemical gradients and fluid flow can strongly influence transport. In this chapter, we describe recent progress in the study of active transport in such complex environments, focusing on two prominent biological systems-bacteria and eukaryotic cells-as archetypes of active matter. We review research findings highlighting how environmental factors can fundamentally alter cellular motility, hindering or promoting active transport in unexpected ways, and giving rise to fascinating behaviors such as directed migration and large-scale clustering. In parallel, we describe specific open questions and promising avenues for future research. Furthermore, given the diverse forms of active matterranging from enzymes and driven biopolymer assemblies, to microorganisms and synthetic microswimmers, to larger animals and even robots-we also describe connections to other active systems as well as more general theoretical/computational models of transport processes in complex environments. * Preprint of a chapter in the book Out-of-Equilibrium Soft Matter: Active Fluids, to be published by the Royal Society of Chemistry.

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Chemotactic smoothing of collective migration

Cited by 36 publications

References 102 publications

Roughening instability of growing 3D bacterial colonies

Roughening instability of growing 3D bacterial colonies

Influence of confinement on the spreading of bacterial populations

Active transport in complex environments

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