Architectural transitions in
            <i>Vibrio cholerae</i>
            biofilms at single-cell resolution

Drescher, Knut; Dunkel, Jörn; Nadell, Carey D.; Teeffelen, Sven van; Grnja, Ivan; Wingreen, Ned S.; Stone, Howard A.; Bassler, Bonnie L.

doi:10.1073/pnas.1601702113

Cited by 188 publications

(233 citation statements)

References 79 publications

(80 reference statements)

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“…We and others recently reported single-cell resolution imaging of fixed bacterial biofilm samples using staining and ensemble averaging (20,21). Because these analyses relied on fixed cells, they could not uncover key temporal information about the biofilm developmental process.…”

Section: Resultsmentioning

confidence: 99%

Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging

Yan

Sharo

Stone

et al. 2016

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

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165

210

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Biofilms are surface-associated bacterial communities that are crucial in nature and during infection. Despite extensive work to identify biofilm components and to discover how they are regulated, little is known about biofilm structure at the level of individual cells. Here, we use state-of-the-art microscopy techniques to enable live singlecell resolution imaging of a Vibrio cholerae biofilm as it develops from one single founder cell to a mature biofilm of 10,000 cells, and to discover the forces underpinning the architectural evolution. Mutagenesis, matrix labeling, and simulations demonstrate that surface adhesion-mediated compression causes V. cholerae biofilms to transition from a 2D branched morphology to a dense, ordered 3D cluster. We discover that directional proliferation of rod-shaped bacteria plays a dominant role in shaping the biofilm architecture in V. cholerae biofilms, and this growth pattern is controlled by a single gene, rbmA. Competition analyses reveal that the dense growth mode has the advantage of providing the biofilm with superior mechanical properties. Our single-cell technology can broadly link genes to biofilm fine structure and provides a route to assessing cell-to-cell heterogeneity in response to external stimuli. biofilm | single cell | self-organization | community | biomechanics

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Section: Resultsmentioning

confidence: 99%

Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging

Yan

Sharo

Stone

et al. 2016

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

Self Cite

165

210

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“…The system (26) is equivalent to taking the limit of D → 0 in (13). Moreover, it is the same first-correction problem that arises in [5,11].…”

Section: Dimensionless Equations We Scale the Variables Viaxmentioning

confidence: 99%

“…If there were specific problems that required nonlinear coupling conditions or an inhomogeneous internal structure to be included, the framework we have developed in this paper could be extended to include such properties, but analytic results are unlikely. With recent advances in high-resolution imaging techniques for bacteria, such as those used in [13], one could develop a more accurate model of the bacterial interior and use experimentally relevant bacterial shapes and distributions of bacteria, allowing the upscaling procedure to be performed on a more accurate description of the microstructure.…”

Section: Higher-order Cell Region Problem Introducing the Dirac Deltmentioning

confidence: 99%

Upscaling Diffusion Through First-Order Volumetric Sinks: A Homogenization of Bacterial Nutrient Uptake

Dalwadi¹,

Wang²,

King³

et al. 2018

SIAM J. Appl. Math.

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Abstract. In mathematical models that include nutrient delivery to bacteria, it is prohibitively expensive to include a pointwise nutrient uptake within small bacterial regions over bioreactor lengthscales, and so such models often impose an effective uptake instead. In this paper, we systematically investigate how the effective uptake should scale with bacterial size and other microscale properties under first-order uptake kinetics. We homogenize the unsteady problem of nutrient diffusing through a locally periodic array of spherical bacteria, within which it is absorbed. We introduce a general model that could also be applied to other single-cell microorganisms, such as cyanobacteria, microalgae, protozoa, and yeast, and we consider generalizations to arbitrary bacterial shapes, including some analytic results for ellipsoidal bacteria. We explore in detail the three distinguished limits of the system on the timescale of diffusion over the macroscale. When the bacterial size is of the same order as the distance between them, the effective uptake has two limiting behaviors, scaling with the bacterial volume for weak uptake and with the bacterial surface area for strong uptake. We derive the function that smoothly transitions between these two behaviors as the system parameters vary. Additionally, we explore the distinguished limit in which bacteria are much smaller than the distance between them and have a very strong uptake. In this limit, we find that the effective uptake is bounded above as the uptake rate grows without bound; we are able to quantify this and characterize the transition to the other limits we consider.

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“…2,4,[13][14][15][16] Improvements in computational analyses allowed quantication of biolm structure for biolms grown in liquid conditions [17][18][19][20] and recent technical advances in high-resolution optical microscopy enabled the investigation of the extracellular matrix structure, 21,22 even at the single cell level. 23 Together, those studies provided crucial information that is urgently needed to prevent or control biolm formation, 9,24 such as the fundamental role of the biolm matrix in establishing emergent biolm properties. 25 While many bacteria produce biolms on surfaces under water-saturated conditions (in liquid), 17,20,23 B. subtilis forms biolms on solid nutrient surfaces in air, or at liquid-air interfaces.…”

Section: Introductionmentioning

confidence: 99%

Matrix composition determines the dimensions of Bacillus subtilis NCIB 3610 biofilm colonies grown on LB agar

et al. 2017

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The production of biomolecules can provide new functionalities to the synthesizing organism. One important example is the secretion of extracellular polymeric substances (EPS) by biofilm forming bacteria. This biofilm matrix protects the individual bacteria within the biofilm from external stressors such as antibiotics, chemicals and shear flow. Previous studies have determined several main matrix components of biofilms formed by Bacillus subtilis. However, how these matrix components influence the growth behavior and final dimensions of B. subtilis biofilms has not yet been determined. Here, we combine different experimental techniques with theoretical modeling to assess this relation. In particular, we quantify the area covered by the biofilm and the biofilm height by performing time-lapse microscopy and light profilometry, respectively. We study the development of biofilms formed by two wild-type strains (B-1 and NCIB 3610) differing in their matrix composition and NCIB 3610 mutant strains lacking the ability to produce specific EPS. Based on the experimentally obtained growth dynamics, we develop a mathematical model that allows us to quantify the influence of three key biofilm matrix components on the final NCIB 3610 biofilm colony dimensions. In detail, we show that two matrix components, the exopolysaccharide produced by the epsA-O operon and the surface layer protein BslA control the area covered by the biofilm colony. The height of these mature biofilm colonies is mostly affected by BslA.Together, our results emphasize the importance of the biofilm matrix composition for biofilm growth and the final dimensions of mature B. subtilis NCIB 3610 biofilm colonies.

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Architectural transitions in Vibrio cholerae biofilms at single-cell resolution

Cited by 188 publications

References 79 publications

Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging

Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging

Upscaling Diffusion Through First-Order Volumetric Sinks: A Homogenization of Bacterial Nutrient Uptake

Matrix composition determines the dimensions of Bacillus subtilis NCIB 3610 biofilm colonies grown on LB agar

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