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 E. Otzen, Per Halkjær Nielsen, Susana Geifman-Shochat, Staffan Kjelleberg, Morten S. Dueholm

Research output: Contribution to journalArticlepeer-review

45 Citations (Scopus)

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-hydroxy-4(1H)-quinolone and N-(3-oxododecanoyl)-L-homoserine lactone, 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 thesametime secure within the extracellular matrix as a consequence of serial bindings. Retention of the QS molecules was confirmed using Pseudomonas aeruginosa PAO1-based 2-heptyl-3-hydroxy-4(1H)-quinolone and N-(3-oxodo-decanoyl)- L-homoserine lactone reporter assays, showing that Fap fibrils pretreated with the QS molecules activate the reporters even after sequential washes. Pyocyanin retention was validated by electrochemical analysis of pyocyanin-pretreated Fap fibrils subjected to the same washing process. Results suggest that QS molecule-amyloid interactions are probably important in the turbulent environments commonly encountered in natural habitats.

Original languageEnglish
Pages (from-to)6457-6469
Number of pages13
JournalJournal of Biological Chemistry
Volume290
Issue number10
DOIs
Publication statusPublished - Mar 6 2015
Externally publishedYes

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

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