Geometry and Mechanics of Microdomains in Growing Bacterial Colonies

You, Zhihong; Pearce, Daniel J.; Sengupta, Anupam; Giomi, Luca

doi:10.1103/physrevx.8.031065

Cited by 98 publications

(157 citation statements)

References 54 publications

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“…From the correlation functions, we see the microscopic arrangement of twitchers to form co-moving polar-aligned pairs in low coverage situations. However, the twitchers self-assemble into oriented local domains at high coverage, which form heterogeneous ordered polydomains within larger liquid-like regions, similar to bacterial rafts observed in bacterial colonies 78 . Biologically observed rafts generally move radially outward from the colony along the local alignment of the cells, which are in tight contact.…”

Section: Discussionmentioning

confidence: 73%

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Collective Dynamics of Model Pili-Based Twitcher-Mode Bacilliforms

Nagel

Greenberg

Shendruk

et al. 2020

Sci Rep

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Pseudomonas aeruginosa, like many bacilliforms, are not limited only to swimming motility but rather possess many motility strategies. in particular, twitching-mode motility employs hair-like pili to transverse moist surfaces with a jittery irregular crawl. twitching motility plays a critical role in redistributing cells on surfaces prior to and during colony formation. We combine molecular dynamics and rule-based simulations to study twitching-mode motility of model bacilliforms and show that there is a critical surface coverage fraction at which collective effects arise. Our simulations demonstrate dynamic clustering of twitcher-type bacteria with polydomains of local alignment that exhibit spontaneous correlated motions, similar to rafts in many bacterial communities. Active matter possesses the potential to bridge between physics and biology. Like living systems, manufactured active systems maintain far-from-equilibrium states by autonomously drawing energy from the surroundings to fuel non-thermal processes. Furthermore, active systems exhibit many of the characteristic traits of biological materials, such as spontaneous motion, self-organization and complex spatio-temporal dynamics. Communities of model bacteria, such as Pseudomonas aeruginosa, are excellent biological examples of out-of-equilibrium systems. These relatively simple living systems serve as a biophysical study of active matter in which collectivity arising from bio-mechanical action can perform essential biological roles. Theories and simulations have approached such bacterial systems by simplifying or omitting all but the most essential, lowest-order physical traits of these microbes, as well as biological complexities. From the very first considerations of active matter, self-propulsion and local alignment were identified as the fundamental components necessary for collective dynamics to emerge from active particles 1,2. Simulations of self-propelled rods and their continuum limit of active nematics have been particularly important to the field 3-14 , as recently reviewed in ref. 15. However, the universality of behaviors exhibited by active systems is still a matter of debate 16,17 and it cannot simply be taken for granted that the collective dynamics of Vicsek boids 1 , active Brownian particles 18-20 or self-propelled rods are directly inherited by microbial motility strategies. Indeed it is known that what might appear to be higher-order details can qualitatively alter the large-scale dynamics. For example, while self-propelled rods and other active colloids commonly exhibit pronounced clustering 21 , which can be explained by motility-induced phase separation or other theoretical approaches 22-24 , swimming microbes can behave as homogeneous fluids on the scales of mesoscale active turbulence 25 , with simulations suggesting that the details of hydrodynamic interactions are essential for differentiating these large-scale swimmer properties 20,26-28. Various modes of swimming motility, including but not limited to pushing, pulling, squi...

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Section: Discussionmentioning

confidence: 73%

“…2b, for example. The locally correlated domains represent proto-rafts, regions of strong nematic ordering that are reminiscent of the "rafts" observed in dense communities P. aeruginosa 78,79 .…”

Section: Solitary Twitchermentioning

confidence: 98%

Collective Dynamics of Model Pili-Based Twitcher-Mode Bacilliforms

Nagel

Greenberg

Shendruk

et al. 2020

Sci Rep

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“…1). Despite the mechanical interactions being more complex in disk-like colonies [11,29], the physical picture emerging from the simulations is nearly identical to that discussed for chain-like colonies.…”

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confidence: 72%

“…Whereas this transition manifests itself in a multitude of possible variants, depending upon the nature of the environmental and intercellular forces, it robustly relies on a limited number of fundamental principles, which most cellular systems have in common. First, the interplay between steric interactions and active motion or growth, drives the formation of coherent structures on the plane, such as nematic domains [11], topological defects [21] or large groups of collectively moving cells [32]. Second, the extensile stresses arising from the in-plane spatial organization and the lack of vertical confinement, drives the cellular layer to be unstable to extrusion.…”

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confidence: 99%

Mono- to Multilayer Transition in Growing Bacterial Colonies

et al. 2019

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The transition from monolayers to multilayered structures in bacterial colonies is a fundamental step in biofilm development. Observed across different morphotypes and species, this transition is triggered within freely growing bacterial microcolonies comprising a few hundred cells. Using a combination of numerical simulations and analytical modeling, here we demonstrate that this transition originates from the competition between growth-induced in-plane active stresses and vertical restoring forces, due to the cell-substrate interactions. Using a simple chain-like colony of laterally confined cells, we show that the transition is triggered by the mechanical instability of individual cells, thus it is localized and mechanically deterministic. Asynchronous cell division renders the process stochastic, so that all the critical parameters that control the onset of the transition are continuously distributed random variables. Upon modeling cell division as a Poisson process, we can approximately calculate the probability distribution function of the position and time associated with the first extrusion. The rate of such a Poisson process can be identified as the order parameter of the transition, thus highlighting its mixed deterministic/stochastic nature.

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“…The urgent need for devising better antibiotics, the development of bioremediation approaches for anthropogenic disasters such as oil spills, application of microbes toward sustainable ecosystems, and the need to coherently assess how microbes govern the dynamics of soil, plant, marine, and human ecosystems-all require an articulate understanding of the vital functions that microbes carry out. Microbial activity spans multiple scales [1][2][3]: from community dynamics playing over millimeter to meter scales, down to sub-cellular organelles with characteristic lengths of hundreds of nanometers (Figure 1). A significant proportion of these microbes-from prokaryotic bacteria making up different biotopes, to eukaryotic phytoplankton in flow-occupy highly dynamic natural habitats, where a combination of periodic and stochastic variations in their micro-environments shape the species fitness, succession, and selection [4,5].…”

Section: Introductionmentioning

confidence: 99%

Microbial Active Matter: A Topological Framework

Sengupta

2020

Front. Phys.

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Topology transcends boundaries that conventionally delineate physical, biological, and engineering sciences. Our ability to mathematically describe topology, combined with recent access to precision tracking and manipulation approaches, has triggered a fresh appreciation of topological ramifications in biological systems. Microbial ecosystems, a classic example of living matter, offer a rich test bed for exploring the role of topological defects in shaping community compositions, structure, and functions spanning orders in length and time scales. Microbial activity-characteristic of such structured, out-of-equilibrium systems-triggers emergent processes that endow evolutionary and ecological benefits to microbial communities. The scene stealer of this developing cross-disciplinary field of research is the topological defects: singularities that nucleate due to spontaneous symmetry breaking within the microbial system or within the surrounding material field. The interplay of geometry, order, and topology elicit novel, if not unexpected dynamics that are at the heart of active and emergent processes in such living systems. In this short review, I have put together a summary of the key recent advances that highlight the interface of active liquid crystal physics and the physical ecology of microbes; and combined it with original data from experiments on sessile species as a case to demonstrate how this interface offers a biophysical framework that could help to decode and harness active microbial processes in true ecological settings. Topology and its functional manifestations-a crucial and well-timed topic-offer a rich opportunity for both experimentalists and theoreticians willing to take up an exciting journey across scales and disciplines.

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Geometry and Mechanics of Microdomains in Growing Bacterial Colonies

Abstract: role of mechanics in the ecophysiology of prokaryotic cells come to the forefront [6,[9][10][11][12][13][14][15][16][17], highlighting the governing biophysical principles that drive colony formation. arXiv:1703.04504v2 [cond-mat.soft]

Cited by 98 publications

References 54 publications

Collective Dynamics of Model Pili-Based Twitcher-Mode Bacilliforms

Collective Dynamics of Model Pili-Based Twitcher-Mode Bacilliforms

Mono- to Multilayer Transition in Growing Bacterial Colonies

Microbial Active Matter: A Topological Framework

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