Engineering microbial physiology with synthetic polymers: cationic polymers induce biofilm formation in<i>Vibrio cholerae</i>and downregulate the expression of virulence genes

Pérez-Soto, Nicolás; Moule, Lauren; Crisan, Daniel N.; Insua, Ignacio; Taylor-Smith, Leanne M.; Voelz, Kerstin; Fernández-Trillo, Francisco; Krachler, Anne Marie

doi:10.1039/c7sc00615b

Cited by 14 publications

(40 citation statements)

References 44 publications

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“…To assess viable bacterial counts at the experimental end point, samples were serially diluted in high-salt buffer to disrupt clusters as previously described, 3f and plated. Similar numbers of colony forming units were recovered from untreated or polymer-treated samples (Figure 1H, I), suggesting that the presence of polymers did not affect bacterial viability or proliferation, in agreement with our previous data.…”

Section: Resultsmentioning

confidence: 99%

“…At low concentrations, cationic polymers are still capable of causing bacterial aggregation by mediating electrostatic interactions, but do so without significantly affecting bacterial membrane integrity and growth. 3…”

Section: Introductionmentioning

confidence: 99%

“…We and others have previously reported that bacteria clustered by sub-inhibitory concentrations of cationic polymers display interesting phenotypes resembling those of biofilm communities. 3 For instance, we have recently demonstrated that clustering of the diarrheal pathogen Vibrio cholerae with methacrylamides containing primary or tertiary amines leads to accumulation of biomass and extracellular DNA, and represses ToxT-regulated virulence factors including cholera toxin. 3f However, what drives these phenotypic changes in response to polymer exposure remains unclear.…”

Section: Introductionmentioning

confidence: 99%

“…3 For instance, we have recently demonstrated that clustering of the diarrheal pathogen Vibrio cholerae with methacrylamides containing primary or tertiary amines leads to accumulation of biomass and extracellular DNA, and represses ToxT-regulated virulence factors including cholera toxin. 3f However, what drives these phenotypic changes in response to polymer exposure remains unclear. Similarly, the marine bacterium Vibrio harveyi shows enhanced bioluminescence in response to polymer-mediated clustering.…”

Section: Introductionmentioning

confidence: 99%

“…Similarly, the marine bacterium Vibrio harveyi shows enhanced bioluminescence in response to polymer-mediated clustering. 3a, 3b, 3e The bacterial components necessary to produce luminescence are encoded by the luxCDABE genes and subject to complex regulatory mechanisms. A major regulatory cascade controlling luminescence is quorum sensing.…”

Section: Introductionmentioning

confidence: 99%

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Aggregation ofVibrio choleraeby cationic polymers enhances quorum sensing but over-rides biofilm dissipation in response to autoinduction

Pérez-Soto

Creese

Fernández-Trillo

et al. 2018

Preprint

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19Vibrio cholerae is a Gram-negative bacterium found in aquatic environments and a human 20 pathogen of global significance. Its transition between host-associated and environmental life 21 styles involves the tight regulation of niche-specific phenotypes such as motility, biofilm formation 22 and virulence. V. cholerae's transition from the host to environmental dispersal usually involves 23 suppression of virulence and dispersion of biofilm communities. In contrast to this naturally 24 occurring transition, bacterial aggregation by cationic polymers triggers a unique response, which 25 is to suppress virulence gene expression while also triggering biofilm formation by V. cholerae, 26 an artificial combination of traits that is potentially very useful to bind and neutralize the pathogen 27 from contaminated water. Here, we set out to uncover the mechanistic basis of this polymer-28 triggered bacterial behavior. We found that bacteria-polymer aggregates undergo rapid 29 autoinduction and achieve quorum sensing at bacterial densities far below those required for 30 autoinduction in the absence of polymers. We demonstrate this induction of quorum sensing is due 31 both to a rapid formation of autoinducer gradients and local enhancement of autoinducer 32 concentrations within bacterial clusters, as well as the stimulation of CAI-1 and AI-2 production 33 by aggregated bacteria. We further found that polymers cause an induction of the biofilm specific 34 regulator VpsR and the biofilm structural protein RbmA, bypassing the usual suppression of 35 biofilm during autoinduction. Overall, this study highlights that synthetic materials can be used to 36 cross-wire natural bacterial responses to achieve a combination of phenotypes with potentially 37 useful applications. 38 39 40 41 Polymers and quorum sensing in V. cholerae 42 Both natural and synthetic cationic macromolecules, such as cationic antimicrobial peptides, 43 cationic polymers and dendrimers, have been extensively reported as antimicrobial. 1 Due to their 44 positive charge, these polymers can efficiently bind the negatively charged envelope of Gram-45 negative and Gram-positive bacteria. 2 At high concentrations and charge densities, these molecules 46 have the potential to interfere with membrane integrity and decrease bacterial viability. 1 However, 47 antimicrobial activity is heavily dependent on the length and nature of the polymer and, more 48 importantly, on the nature of the targeted microbe. At low concentrations, cationic polymers are 49 still capable of causing bacterial aggregation by mediating electrostatic interactions, but do so 50 without significantly affecting bacterial membrane integrity and growth. 3 51 We and others have previously reported that bacteria clustered by sub-inhibitory 52 concentrations of cationic polymers display interesting phenotypes resembling those of biofilm 53 communities. 3 For instance, we have recently demonstrated that clustering of the diarrheal 54 pathogen Vibrio cholerae with methacrylamides containing primar...

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Aggregation ofVibrio choleraeby cationic polymers enhances quorum sensing but over-rides biofilm dissipation in response to autoinduction

Pérez-Soto

Creese

Fernández-Trillo

et al. 2018

Preprint

Self Cite

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A Supramolecular Approach to Engineering Living Cells with Enzymes for Adaptive and Recyclable Cascade Synthesis

Wang,

Hübner,

Karring

et al. 2024

Angewandte Chemie

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Biocatalytic transformation in nature is inherently dynamic, spontaneous, and adaptive, enabling complex chemical synthesis and metabolism. These processes often involve supramolecular recognition among cells, enzymes, and biomacromolecules, far surpassing the capabilities of isolated cells and enzymes used in industrial synthesis. Inspired by nature, here we design a supramolecular approach to equip living cells with these capacities, enabling recyclable, efficient cascade reactions. Our two‐step "plug‐and‐play" methodology begins by coating Escherichia coli cells with guest‐containing polymers (SupraBAC) via supramolecular charge interactions, followed by the introduction of β‐cyclodextrin‐functionalized host enzymes through host‐guest chemistry, creating a robust cell‐enzyme complex. This supramolecular coating not only protects cells from various stresses, such as UV radiation, heat, and organic solvents, but also facilitates the overexpression of intracellular enzymes and the attachment of extracellular enzymes within and on SupraBAC. This combination results in efficient multienzyme cascade synthesis, enabling two‐ and three‐step reactions in one pot. Importantly, the multienzyme system can be recycled up to five times without significant loss of activity. Our findings introduce a versatile, adaptive supramolecular coating for whole‐cell catalysts, offering a sustainable and efficient solution for complex synthesis in both chemistry and industrial biotechnology.

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A Supramolecular Approach to Engineering Living Cells with Enzymes for Adaptive and Recyclable Cascade Synthesis

Wang,

Hübner,

Karring

et al. 2024

Angew Chem Int Ed

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Engineering microbial physiology with synthetic polymers: cationic polymers induce biofilm formation inVibrio choleraeand downregulate the expression of virulence genes

Abstract: Here we report the first application of non-bactericidal synthetic polymers to modulate the physiology of a bacterial pathogen.

Cited by 14 publications

References 44 publications

Aggregation ofVibrio choleraeby cationic polymers enhances quorum sensing but over-rides biofilm dissipation in response to autoinduction

Aggregation ofVibrio choleraeby cationic polymers enhances quorum sensing but over-rides biofilm dissipation in response to autoinduction

A Supramolecular Approach to Engineering Living Cells with Enzymes for Adaptive and Recyclable Cascade Synthesis

A Supramolecular Approach to Engineering Living Cells with Enzymes for Adaptive and Recyclable Cascade Synthesis

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