Confinement-induced self-organization in growing bacterial colonies

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

doi:10.1126/sciadv.abc8685

Cited by 51 publications

(55 citation statements)

References 44 publications

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“…Biofilm formation is a morphogenetic process whereby a single founder cell develops into a threedimensional (3D) aggregate in which bacterial cells interact with each other and with the environment (4)(5)(6)(7)(8). Recent work has revealed biophysical mechanisms underlying biofilm morphogenesis on solid substrates, which is controlled by cell-substrate adhesion and the resulting shear stress (9)(10)(11)(12)(13)(14)(15). In addition to those living on surfaces, bacterial communities are also commonly found inside soft, structured environments, such as hydrogels.…”

mentioning

confidence: 99%

Morphogenesis and cell ordering in confined bacterial biofilms

Zhang

Nijjer

et al. 2021

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

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Biofilms are aggregates of bacterial cells surrounded by an extracellular matrix. Much progress has been made in studying biofilm growth on solid substrates; however, little is known about the biophysical mechanisms underlying biofilm development in three-dimensional confined environments in which the biofilm-dwelling cells must push against and even damage the surrounding environment to proliferate. Here, combining single-cell imaging, mutagenesis, and rheological measurement, we reveal the key morphogenesis steps of Vibrio cholerae biofilms embedded in hydrogels as they grow by four orders of magnitude from their initial size. We show that the morphodynamics and cell ordering in embedded biofilms are fundamentally different from those of biofilms on flat surfaces. Treating embedded biofilms as inclusions growing in an elastic medium, we quantitatively show that the stiffness contrast between the biofilm and its environment determines biofilm morphology and internal architecture, selecting between spherical biofilms with no cell ordering and oblate ellipsoidal biofilms with high cell ordering. When embedded in stiff gels, cells self-organize into a bipolar structure that resembles the molecular ordering in nematic liquid crystal droplets. In vitro biomechanical analysis shows that cell ordering arises from stress transmission across the biofilm–environment interface, mediated by specific matrix components. Our imaging technique and theoretical approach are generalizable to other biofilm-forming species and potentially to biofilms embedded in mucus or host tissues as during infection. Our results open an avenue to understand how confined cell communities grow by means of a compromise between their inherent developmental program and the mechanical constraints imposed by the environment.

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confidence: 99%

Morphogenesis and cell ordering in confined bacterial biofilms

Zhang

Nijjer

et al. 2021

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

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“…However, these assumptions are not unreasonable: Our choice of the domain and boundary conditions was motivated by rectangular microfluidic traps used routinely by synthetic biologists [ 15 ]. The prevalent nematic ordering of cells in close-packed environments that is central to the emergence of spatio-temporal patterns has been observed experimentally [ 32 , 37 , 45 , 59 ], and has been examined numerically [ 32 , 48 , 59 ] and analytically [ 32 – 34 , 47 , 48 ]. Although such nematic order is most likely to emerge in monolayer traps, it has been observed in colonies growing in three dimensions [ 54 ].…”

Section: Discussionmentioning

confidence: 99%

Emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia

et al. 2021

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The increased complexity of synthetic microbial biocircuits highlights the need for distributed cell functionality due to concomitant increases in metabolic and regulatory burdens imposed on single-strain topologies. Distributed systems, however, introduce additional challenges since consortium composition and spatiotemporal dynamics of constituent strains must be robustly controlled to achieve desired circuit behaviors. Here, we address these challenges with a modeling-based investigation of emergent spatiotemporal population dynamics using cell-length control in monolayer, two-strain bacterial consortia. We demonstrate that with dynamic control of a strain’s division length, nematic cell alignment in close-packed monolayers can be destabilized. We find that this destabilization confers an emergent, competitive advantage to smaller-length strains—but by mechanisms that differ depending on the spatial patterns of the population. We used complementary modeling approaches to elucidate underlying mechanisms: an agent-based model to simulate detailed mechanical and signaling interactions between the competing strains, and a reductive, stochastic lattice model to represent cell-cell interactions with a single rotational parameter. Our modeling suggests that spatial strain-fraction oscillations can be generated when cell-length control is coupled to quorum-sensing signaling in negative feedback topologies. Our research employs novel methods of population control and points the way to programming strain fraction dynamics in consortial synthetic biology.

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“…7). In fact, long-range order can be induced whenever a 2D growing bacterial colony deviates from an isotropically expanding pattern, for instance when confined in a rectangular geometry 42,43 or during inward growth 34 . This model thus reveals that differential growth, established by a verticalized core ( r 0 ≠ 0), generates the driving force for radial alignment in a growing biofilm.…”

Section: Cholerae Biofilms Self-organize Into Aster Patternsmentioning

confidence: 99%

Biofilm self-patterning: mechanical forces drive a reorientation cascade

Nijjer

Zhang

et al. 2021

Preprint

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During development, cells often self-organize into distinctive patterns with long-range orientational order. However, the mechanism by which long-range order emerges through complex interactions, particularly in the prokaryotic domain, remains elusive. Here we report, in growing Vibrio cholerae biofilms, a reorientation cascade consisting of cell verticalization in the core and radial alignment in the rim, generating a pattern reminiscent of a blooming aster. Single-cell imaging combined with agent-based simulations reveal that cell verticalization and radial alignment are spatiotemporally coupled, each generating the driving force for the other, to cause a dynamic cascade of differential orientational ordering. Such self-patterning is absent in nonadherent mutants but can be restored through opto-manipulation of growth. A two-phase active nematic model is developed to elucidate the mechanism underlying biofilm self-patterning, which offers insights into the control of organization in complex bacterial communities.

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Confinement-induced self-organization in growing bacterial colonies

Cited by 51 publications

References 44 publications

Morphogenesis and cell ordering in confined bacterial biofilms

Morphogenesis and cell ordering in confined bacterial biofilms

Emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia

Biofilm self-patterning: mechanical forces drive a reorientation cascade

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