Aggregation by depletion attraction in cultures of bacteria producing exopolysaccharide

Dorken, Gary; Ferguson, Gail P.; French, Christopher C.; Poon, Wilson

doi:10.1098/rsif.2012.0498

Cited by 83 publications

(93 citation statements)

References 55 publications

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“…In a recent experiment, a bacterial strain with EPS overproduction (specifically, exopolysaccharide succinoglycan in the S. meliloti bacteria) (38) clearly shows evidence that bacterial cells can form small clusters; an image of their experiment is shown in Fig. 8A.…”

Section: Resultsmentioning

confidence: 97%

“…The origin of this depletion effect is an entropy gain due to the increased accessible volume of the small depleting EPS particles when large objects (bacterial cells) approach one another and reduce the excluded volume for the depletants. Inspired by recent experimental finding of Dorken and coworkers (38) of enhanced aggregation and phase separation of a mutant bacterium Sinorhizobium meliloti that overproduces EPSs, we study the effect of EPS particles in the growing bacterial colony.…”

Section: Resultsmentioning

confidence: 99%

“…Instead, we approximate the EPSs as small spherical particles having a radius equal to their radius of gyration (38,39). For the sake of computational ease, we will typically take this radius to be around half that of a bacterial cell (38), as shown in Fig. 1.…”

Section: The Model and Methodsmentioning

confidence: 99%

“…(30-34). Recently, a number of studies revealed that crowding effects by extracellular substances can operate in bacterial cultures as well (35)(36)(37)(38)(39)(40). However, these earlier works study the role of depletion attraction operating in an equilibrium mixture of fixed bacterial cells and polymer concentration.…”

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confidence: 99%

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Mechanically-driven phase separation in a growing bacterial colony

Ghosh

Mondal

Ben‐Jacob

et al. 2015

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

114

163

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Secretion of extracellular polymeric substances (EPSs) by growing bacteria is an integral part of forming biofilm-like structures. In such dense systems, mechanical interactions among the structural components can be expected to significantly contribute to morphological properties. Here, we use a particle-based modeling approach to study the self-organization of nonmotile rod-shaped bacterial cells growing on a solid substrate in the presence of selfproduced EPSs. In our simulation, all of the components interact mechanically via repulsive forces, occurring as the bacterial cells grow and divide (via consuming diffusing nutrient) and produce EPSs. Based on our simulation, we show that mechanical interactions control the collective behavior of the system. In particular, we find that the presence of nonadsorbing EPSs can lead to spontaneous aggregation of bacterial cells by a depletion attraction and thereby generates phase separated patterns in the nonequilibrium growing colony. Both repulsive interactions between cell and EPSs and the overall concentration of EPSs are important factors in the self-organization in a nonequilibrium growing colony. Furthermore, we investigate the interplay of mechanics with the nutrient diffusion and consumption by bacterial cells and observe that suppression of branch formation occurs due to EPSs compared with the case where no EPS is produced.A common underlying theme of biophysics of living matter is the quest to understand how local interactions of individual components lead to collective behavior and formation of highly self-organized systems (1-6). In this regard, bacterial systems are an especially interesting example. Bacteria are known to selforganize into multicellular communities, commonly known as biofilms, in which microbial cells live in close association with a solid surface or liquid-air interface and are embedded in a self-produced extracellular matrix. Extracellular polymeric substances (EPSs) play an important role in determining the structural and mechanical architecture of a biofilm (7-12). Generally, the collective dynamics of bacterial colony involves a complex interplay of various physical, chemical, and biological mechanisms, such as growth and differentiation of cells, production of EPSs, the collective movement of cells determined by interacting physical forces and chemical cues, e.g., chemotaxis, motility, cellcell signaling, adhesion, and gene regulation (13)(14)(15)(16)(17)(18)(19). At low density, communication among cells occurs mainly through chemical signals (20). However, at a higher density, as bacteria aggregate and form dense communities, direct mechanical interaction becomes increasingly relevant in the self-organization (21-23). In this regard, microfluidics-based experiments coupled with continuum modeling of cellular dynamics by Volfson et al.(24) was a pioneering study emphasizing the role of cell-cell mechanical interaction in the growth of a highly organized bacterial colony. As a significant extension, Farrell and coworkers (25, 26) hav...

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Section: Resultsmentioning

confidence: 97%

Section: Resultsmentioning

confidence: 99%

Section: The Model and Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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Mechanically-driven phase separation in a growing bacterial colony

Ghosh

Mondal

Ben‐Jacob

et al. 2015

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

114

163

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“…Here, we have combined physical/chemical studies of the organism and mutant strains with quantitative modelling to investigate the surface spreading. We find that two purely entropy-driven phenomena-osmotic flow [14] and the depletion (crowding) attraction [15][16][17]-attributable to the exopolysaccharide EPS II drive the physical dispersion of the colony. An osmotic model captures the observed kinetics and parameterdependence of colony spreading, whereas flagellar swimming plays a more secondary role of maintaining the mucoid suspension of cells.…”

Section: Introductionmentioning

confidence: 99%

Entropy-driven motility of Sinorhizobium meliloti on a semi-solid surface

2014

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Sinorhizobium meliloti growing on soft agar can exhibit an unusual surface spreading behaviour that differs from other bacterial surface motilities. Bacteria in the colony secrete an exopolysaccharide-rich mucoid fluid that expands outward on the surface, carrying within it a suspension of actively dividing cells. The moving slime disperses the cells in complex and dynamic patterns indicative of simultaneous bacterial growth, swimming and aggregation. We find that while flagellar swimming is required to maintain the cells in suspension, the spreading and the associated pattern formation are primarily driven by the secreted exopolysaccharide EPS II, which creates two entropy-increasing effects: an osmotic flow of water from the agar to the mucoid fluid and a crowding or depletion attraction between the cells. Activation of these physical/chemical phenomena may be a useful function for the high molecular weight EPS II, a galactoglucan whose biosynthesis is tightly regulated by the ExpR/SinI/SinR quorum-sensing system: unlike bacterial colonies that spread via bacterium-generated, physical propulsive forces, S. meliloti under quorum conditions may use EPS II to activate purely entropic forces within its environment, so that it can disperse by passively 'surfing' on those forces.

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Coaggregative interactions between rhizobacteria are promoted by exopolysaccharides from Sinorhizobium meliloti

et al. 2023

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Bacterial surface components and extracellular compounds such as exopolysaccharides (EPSs) are crucial for interactions between cells, tolerance to different types of stress, and host colonization. Sinorhizobium meliloti produces two EPSs: Succinoglycan (EPS I), which is involved in the establishment of symbiosis with Medicago sativa, and galactoglucan (EPS II), associated with biofilm formation and the promotion of aggregation. Here, we aimed to assess their role in aggregative interactions between cells of the same strain of a given species (auto‐aggregation), and between genetically different strains of the same or different species (intra‐ or intergeneric coaggregation). To do this, we used S. meliloti mutants which are defective in the production of EPS I, EPS II, or both. Macroscopic and microscopic coaggregation tests were performed with combinations or pairs of different bacterial strains. The EPS II‐producing strains were more capable of coaggregation than those that cannot produce EPS II. This was true both for coaggregations between different S. meliloti strains, and between S. meliloti and other common rhizobacteria of agricultural relevance, such as Pseudomonas fluorescens and Azospirillum brasilense. The exogenous addition of EPS II strongly promoted coaggregation, thus confirming the polymer's importance for this phenotype. EPS II may therefore be a key factor in events of physiological significance for environmental survival, such as aggregative interactions and biofilm development. Furthermore, it might be a connecting molecule with relevant properties at an ecological, biotechnological, and agricultural level.

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Aggregation by depletion attraction in cultures of bacteria producing exopolysaccharide

Cited by 83 publications

References 55 publications

Mechanically-driven phase separation in a growing bacterial colony

Mechanically-driven phase separation in a growing bacterial colony

Entropy-driven motility of Sinorhizobium meliloti on a semi-solid surface

Coaggregative interactions between rhizobacteria are promoted by exopolysaccharides from Sinorhizobium meliloti

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