Quorum sensing signalling alters virulence potential and population dynamics in complex microbiome-host interactomes

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dc.contributor.authorReen, F. Jerry
dc.contributor.authorGutiérrez-Barranquero, José A.
dc.contributor.authorMcCarthy, Ronan R.
dc.contributor.authorWoods, David F.
dc.contributor.authorScarciglia, Sara
dc.contributor.authorAdams, Claire
dc.contributor.authorFog Nielsen, Kristian
dc.contributor.authorGram, Lone
dc.contributor.authorO'Gara, Fergal
dc.contributor.funderEnterprise Irelanden
dc.contributor.funderHealth Research Boarden
dc.contributor.funderEuropean Commissionen
dc.contributor.funderScience Foundation Irelanden
dc.contributor.funderIrish Research Council for Science, Engineering and Technologyen
dc.contributor.funderCystic Fibrosis Foundationen
dc.contributor.funderAgilent Technologiesen
dc.date.accessioned2019-10-14T21:37:23Z
dc.date.available2019-10-14T21:37:23Z
dc.date.issued2019-09-11
dc.description.abstractDespite the discovery of the first N-acyl homoserine lactone (AHL) based quorum sensing (QS) in the marine environment, relatively little is known about the abundance, nature and diversity of AHL QS systems in this diverse ecosystem. Establishing the prevalence and diversity of AHL QS systems and how they may influence population dynamics within the marine ecosystem, may give a greater insight into the evolution of AHLs as signaling molecules in this important and largely unexplored niche. Microbiome profiling of Stelletta normani and BD1268 sponge samples identified several potential QS active genera. Subsequent biosensor-based screening of a library of 650 marine sponge bacterial isolates identified 10 isolates that could activate at least one of three AHL biosensor strains. Each was further validated and profiled by Ultra-High Performance Liquid Chromatography Mass Spectrometry, with AHLs being detected in 8 out of 10 isolate extracts. Co-culture of QS active isolates with S. normani marine sponge samples led to the isolation of genera such as Pseudomonas and Paenibacillus, both of which were low abundance in the S. normani microbiome. Surprisingly however, addition of AHLs to isolates harvested following co-culture did not measurably affect either growth or biofilm of these strains. Addition of supernatants from QS active strains did however impact significantly on biofilm formation of the marine Bacillus sp. CH8a sporeforming strain suggesting a role for QS systems in moderating the microbe-microbe interaction in marine sponges. Genome sequencing and phylogenetic analysis of a QS positive Psychrobacter isolate identified several QS associated systems, although no classical QS synthase gene was identified. The stark contrast between the biodiverse sponge microbiome and the relatively limited diversity that was observed on standard culture media, even in the presence of QS active compounds, serves to underscore the extent of diversity that remains to be brought into culture.en
dc.description.sponsorshipEnterprise Ireland (CF-2017-0757-P); Health Research Board/Irish Thoracic Society (MRCG-2018-6, MRCG-2014-6); Science Foundation Ireland (SSPC-2); Irish Research Council for Science, Engineering and Technology (GOIPG/2014/647); Cystic Fibrosis Foundation, United States (OG1710); Agilent technologies (Thought Leader Donation of the UHPLC-QTOF system)en
dc.description.statusPeer revieweden
dc.description.versionPublished Versionen
dc.format.mimetypeapplication/pdfen
dc.identifier.articleid2131en
dc.identifier.citationReen, F. J., Gutiérrez-Barranquero, J. A., McCarthy, R. R., Woods, D. F., Scarciglia, S., Adams, C., Fog Nielsen, K., Gram, L. and O’Gara, F. (2019) 'Quorum Sensing Signaling Alters Virulence Potential and Population Dynamics in Complex Microbiome-Host Interactomes', Frontiers in Microbiology, 10, 2131 (13pp.). DOI: 10.3389/fmicb.2019.02131en
dc.identifier.doi10.3389/fmicb.2019.02131en
dc.identifier.endpage13en
dc.identifier.issn1664-302X
dc.identifier.journaltitleFrontiers in Microbiologyen
dc.identifier.startpage1en
dc.identifier.urihttps://hdl.handle.net/10468/8751
dc.identifier.volume10en
dc.language.isoenen
dc.publisherFrontiers Mediaen
dc.relation.projectinfo:eu-repo/grantAgreement/SFI/SFI Technology and Innovation Development Award (TIDA)/15/TIDA/2977/IE/Pre-clinical testing of novel fungal biofilm blockers for the medical device sector./en
dc.relation.projectinfo:eu-repo/grantAgreement/EC/H2020::IA/634486/EU/Industrial Applications of Marine Enzymes: Innovative screening and expression platforms to discover and use the functional protein diversity from the sea/INMAREen
dc.relation.urihttps://www.frontiersin.org/articles/10.3389/fmicb.2019.02131/full
dc.rights©2019 Reen, Gutiérrez-Barranquero, McCarthy, Woods, Scarciglia, Adams, Fog Nielsen, Gram and O’Gara. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.en
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.subjectQuorum sensing (QS)en
dc.subjectMicrobiomeen
dc.subjectMarine sponge bacteriaen
dc.subjectCell-cell communicationen
dc.subjectAcyl homoserine lactone (AHLen
dc.titleQuorum sensing signalling alters virulence potential and population dynamics in complex microbiome-host interactomesen
dc.typeArticle (peer-reviewed)en
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