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Effects on membrane lateral pressure suggest permeation mechanisms for bacterial quorum signaling molecules.

ABSTRACT: Quorum sensing is an intricate example of "social" behavior in microbial communities mediated by small secreted molecules (autoinducers). The mechanisms of membrane permeation remain elusive for many of them. Here we present the assessment of membrane permeability for three natural autoinducers and four synthetic analogues based on their polarity, surface activity, affinity for lipid monolayers, and ability to induce lateral pressure changes in the inner E. coli membrane sensed by the bacterial tension-activated channel MscS. AI-1 (N-(3-oxodecanoyl)-l-homoserine lactone) is surface-active, and it robustly inserts into lipid monolayers, indicating strong propensity toward membranes. When presented to membrane patches from the cytoplasmic side, AI-1 transiently shifts MscS's activation curve toward higher tensions due to intercalation into the cytoplasmic leaflet followed by redistribution to the opposite side. Indole showed no detectable surface activity at the air-water interface but produced a moderate increase of lateral pressure in monolayers and was potent at shifting activation curves of MscS, demonstrating transients on sequential additions. AI-2 (4,5-dihydroxy-2,3-pentanedione, DPD) showed little activity at the interfaces, correspondingly with no effect on MscS activation. After chemical modification with isobutyl, hexyl, or heptyl chains, AI-2 displayed strong surface activity. Hexyl and especially heptyl AI-2 induced robust transient shifts of MscS activation curves. The data strongly suggest that both AI-1 and indole are directly permeable through the membrane. AI-2, more hydrophilic, shows low affinity toward lipids and thus requires a transport system, whereas alkyl analogues of AI-2 should permeate the membrane directly.

SUBMITTER: Kamaraju K

PROVIDER: S-EPMC3163381 | biostudies-literature | 2011 Aug

REPOSITORIES: biostudies-literature

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Effects on membrane lateral pressure suggest permeation mechanisms for bacterial quorum signaling molecules.

Kamaraju Kishore K Smith Jacqueline J Wang Jingxin J Roy Varnika V Sintim Herman O HO Bentley William E WE Sukharev Sergei S

Biochemistry 20110721 32

Quorum sensing is an intricate example of "social" behavior in microbial communities mediated by small secreted molecules (autoinducers). The mechanisms of membrane permeation remain elusive for many of them. Here we present the assessment of membrane permeability for three natural autoinducers and four synthetic analogues based on their polarity, surface activity, affinity for lipid monolayers, and ability to induce lateral pressure changes in the inner E. coli membrane sensed by the bacterial ...[more]

PMID: 21736305

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Project description:Kaposi's sarcoma-associated herpesvirus (KSHV) can cause several human cancers, including primary effusion lymphoma (PEL), which frequently occur in immunocompromised patients. KSHV-infected patients often suffer from polymicrobial infections caused by opportunistic bacterial pathogens. Therefore, it is crucial to understand how these coinfecting microorganisms or their secreted metabolites may affect KSHV infection and the pathogenesis of virus-associated malignancies. Quorum sensing (QS), a cell density-based intercellular communication system, employs extracellular diffusible signaling molecules to regulate bacterial virulence mechanisms in a wide range of bacterial pathogens, such as Pseudomonas aeruginosa, which is one of the most common opportunistic microorganisms found in immunocompromised individuals. In this study, we evaluated and compared the influence on PEL growth and the host/viral interactome of the major QS signaling molecules [N-(3-oxododecanoyl)-l-homoserine lactone (OdDHL), N-butyrylhomoserine lactone (BHL), and 2-heptyl-3-hydroxy-4-quinolone (PQS)] in conditioned medium from wild-type (wt) and QS mutant laboratory strains as well as clinical isolates of P. aeruginosa Our data indicate that P. aeruginosa coinfection may facilitate virus dissemination and establishment of new infection and further promote tumor development through effectively inducing viral lytic gene expression by its QS systems.IMPORTANCE Currently, most studies about KSHV infection and/or virus-associated malignancies depend on pure culture systems or immunodeficient animal models. However, the real situation should be much more complicated in KSHV-infected immunocompromised patients due to frequent polymicrobial infections. It is important to understand the interaction of KSHV and coinfecting microorganisms, especially opportunistic bacterial pathogens. Here we report for the first time that P. aeruginosa and its quorum-sensing signaling molecules display a complicated impact on KSHV-associated lymphoma growth as well as the intracellular host/viral gene expression profile. Our data imply that targeting of coinfecting pathogens is probably necessary during treatment of virus-associated malignancies in these immunocompromised patients.

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Effects on membrane lateral pressure suggest permeation mechanisms for bacterial quorum signaling molecules.

Publications

Effects on membrane lateral pressure suggest permeation mechanisms for bacterial quorum signaling molecules.

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