Functional Amyloids Keep Quorum Sensing Molecules in Check

Thomas Seviour; Susan Hove Hansen; Liang Yang; Yin Hoe Yau; Victor Bochuan Wang; Marcel R Stenvang; Gunna Christiansen; Enrico Marsili; Michael Givskov; Yicai Chen; Daniel Otzen; Per Halkjaer Nielsen; Susana Geifman Shochat; Staffan Kjelleberg; Morten Simonsen Dueholm

doi:10.1074/jbc.M114.613810

Functional Amyloids Keep Quorum Sensing Molecules in Check

Thomas Seviour, Susan Hove Hansen, Liang Yang, Yin Hoe Yau, Victor Bochuan Wang, Marcel R Stenvang, Gunna Christiansen, Enrico Marsili, Michael Givskov, Yicai Chen, Daniel Otzen, Per Halkjaer Nielsen, Susana Geifman Shochat, Staffan Kjelleberg, Morten Simonsen Dueholm

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Abstract

The mechanism by which extracellular metabolites including redox mediators and quorum sensing signaling molecules, traffic through the extracellular matrix of biofilms is poorly explored. We hypothesize that functional amyloids, abundant in natural biofilms and possessing hydrophobic domains, retain these metabolites. Using surface plasmon resonance, we demonstrate that the quorum sensing (QS) molecules, 2-heptyl-3,4- dihydroxyquinoline (PQS) and N-(3- oxododecanoyl)-L-homoserine lactone (3-oxo- C12-HSL), and the redox mediator pyocyanin bind with transient affinity to functional amyloids from Pseudomonas (Fap). Their high hydrophobicity predisposes them to signal- amyloid interactions, but specific interactions also play a role. Transient interactions allow for rapid association and dissociation kinetics, which make the QS molecules bioavailable and at the same time secure within the extracellular matrix as a consequence of serial bindings. Retention of the QS molecules was confirmed using P. aeruginosa PAO1 based PQS and 3-oxo-C12-HSL reporter assays, showing that Fap fibrils pre-treated with the QS molecules activate the reporters even after sequential washes. Pyocyanin retention was validated by electrochemical analysis of pyocyanin pre-treated Fap fibrils subjected to the same washing process. Results suggest that QS molecules-amyloid interactions are probably important in turbulent environments commonly encountered in natural habitats.

Original language	English
Journal	Journal of Biological Chemistry
Volume	290
Pages (from-to)	6457-6469
Number of pages	13
ISSN	0021-9258
DOIs	https://doi.org/10.1074/jbc.M114.613810
Publication status	Published - 13 Jan 2015

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title = "Functional Amyloids Keep Quorum Sensing Molecules in Check",

abstract = "The mechanism by which extracellular metabolites including redox mediators and quorum sensing signaling molecules, traffic through the extracellular matrix of biofilms is poorly explored. We hypothesize that functional amyloids, abundant in natural biofilms and possessing hydrophobic domains, retain these metabolites. Using surface plasmon resonance, we demonstrate that the quorum sensing (QS) molecules, 2-heptyl-3,4- dihydroxyquinoline (PQS) and N-(3- oxododecanoyl)-L-homoserine lactone (3-oxo- C12-HSL), and the redox mediator pyocyanin bind with transient affinity to functional amyloids from Pseudomonas (Fap). Their high hydrophobicity predisposes them to signal- amyloid interactions, but specific interactions also play a role. Transient interactions allow for rapid association and dissociation kinetics, which make the QS molecules bioavailable and at the same time secure within the extracellular matrix as a consequence of serial bindings. Retention of the QS molecules was confirmed using P. aeruginosa PAO1 based PQS and 3-oxo-C12-HSL reporter assays, showing that Fap fibrils pre-treated with the QS molecules activate the reporters even after sequential washes. Pyocyanin retention was validated by electrochemical analysis of pyocyanin pre-treated Fap fibrils subjected to the same washing process. Results suggest that QS molecules-amyloid interactions are probably important in turbulent environments commonly encountered in natural habitats.",

author = "Thomas Seviour and Hansen, {Susan Hove} and Liang Yang and Yau, {Yin Hoe} and Wang, {Victor Bochuan} and Stenvang, {Marcel R} and Gunna Christiansen and Enrico Marsili and Michael Givskov and Yicai Chen and Daniel Otzen and Nielsen, {Per Halkjaer} and Shochat, {Susana Geifman} and Staffan Kjelleberg and Dueholm, {Morten Simonsen}",

note = "Copyright {\textcopyright} 2015, The American Society for Biochemistry and Molecular Biology.",

year = "2015",

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doi = "10.1074/jbc.M114.613810",

language = "English",

volume = "290",

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journal = "Journal of Biological Chemistry",

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T1 - Functional Amyloids Keep Quorum Sensing Molecules in Check

AU - Seviour, Thomas

AU - Hansen, Susan Hove

AU - Yang, Liang

AU - Yau, Yin Hoe

AU - Wang, Victor Bochuan

AU - Stenvang, Marcel R

AU - Christiansen, Gunna

AU - Marsili, Enrico

AU - Givskov, Michael

AU - Chen, Yicai

AU - Otzen, Daniel

AU - Nielsen, Per Halkjaer

AU - Shochat, Susana Geifman

AU - Kjelleberg, Staffan

AU - Dueholm, Morten Simonsen

PY - 2015/1/13

Y1 - 2015/1/13

N2 - The mechanism by which extracellular metabolites including redox mediators and quorum sensing signaling molecules, traffic through the extracellular matrix of biofilms is poorly explored. We hypothesize that functional amyloids, abundant in natural biofilms and possessing hydrophobic domains, retain these metabolites. Using surface plasmon resonance, we demonstrate that the quorum sensing (QS) molecules, 2-heptyl-3,4- dihydroxyquinoline (PQS) and N-(3- oxododecanoyl)-L-homoserine lactone (3-oxo- C12-HSL), and the redox mediator pyocyanin bind with transient affinity to functional amyloids from Pseudomonas (Fap). Their high hydrophobicity predisposes them to signal- amyloid interactions, but specific interactions also play a role. Transient interactions allow for rapid association and dissociation kinetics, which make the QS molecules bioavailable and at the same time secure within the extracellular matrix as a consequence of serial bindings. Retention of the QS molecules was confirmed using P. aeruginosa PAO1 based PQS and 3-oxo-C12-HSL reporter assays, showing that Fap fibrils pre-treated with the QS molecules activate the reporters even after sequential washes. Pyocyanin retention was validated by electrochemical analysis of pyocyanin pre-treated Fap fibrils subjected to the same washing process. Results suggest that QS molecules-amyloid interactions are probably important in turbulent environments commonly encountered in natural habitats.

AB - The mechanism by which extracellular metabolites including redox mediators and quorum sensing signaling molecules, traffic through the extracellular matrix of biofilms is poorly explored. We hypothesize that functional amyloids, abundant in natural biofilms and possessing hydrophobic domains, retain these metabolites. Using surface plasmon resonance, we demonstrate that the quorum sensing (QS) molecules, 2-heptyl-3,4- dihydroxyquinoline (PQS) and N-(3- oxododecanoyl)-L-homoserine lactone (3-oxo- C12-HSL), and the redox mediator pyocyanin bind with transient affinity to functional amyloids from Pseudomonas (Fap). Their high hydrophobicity predisposes them to signal- amyloid interactions, but specific interactions also play a role. Transient interactions allow for rapid association and dissociation kinetics, which make the QS molecules bioavailable and at the same time secure within the extracellular matrix as a consequence of serial bindings. Retention of the QS molecules was confirmed using P. aeruginosa PAO1 based PQS and 3-oxo-C12-HSL reporter assays, showing that Fap fibrils pre-treated with the QS molecules activate the reporters even after sequential washes. Pyocyanin retention was validated by electrochemical analysis of pyocyanin pre-treated Fap fibrils subjected to the same washing process. Results suggest that QS molecules-amyloid interactions are probably important in turbulent environments commonly encountered in natural habitats.

U2 - 10.1074/jbc.M114.613810

DO - 10.1074/jbc.M114.613810

M3 - Journal article

C2 - 25586180

SN - 0021-9258

VL - 290

SP - 6457

EP - 6469

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

ER -

Functional Amyloids Keep Quorum Sensing Molecules in Check

Abstract

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