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Quorum Sensing Signaling Alters Virulence Potential and Population Dynamics in Complex Microbiome-Host Interactomes

Despite 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 ho...

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Autores principales: Reen, F. Jerry, Gutiérrez-Barranquero, José A., McCarthy, Ronan R., Woods, David F., Scarciglia, Sara, Adams, Claire, Fog Nielsen, Kristian, Gram, Lone, O’Gara, Fergal
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6749037/
https://www.ncbi.nlm.nih.gov/pubmed/31572336
http://dx.doi.org/10.3389/fmicb.2019.02131
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author Reen, F. Jerry
Gutiérrez-Barranquero, José A.
McCarthy, Ronan R.
Woods, David F.
Scarciglia, Sara
Adams, Claire
Fog Nielsen, Kristian
Gram, Lone
O’Gara, Fergal
author_facet Reen, F. Jerry
Gutiérrez-Barranquero, José A.
McCarthy, Ronan R.
Woods, David F.
Scarciglia, Sara
Adams, Claire
Fog Nielsen, Kristian
Gram, Lone
O’Gara, Fergal
author_sort Reen, F. Jerry
collection PubMed
description Despite 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.
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spelling pubmed-67490372019-09-30 Quorum Sensing Signaling Alters Virulence Potential and Population Dynamics in Complex Microbiome-Host Interactomes Reen, F. Jerry Gutiérrez-Barranquero, José A. McCarthy, Ronan R. Woods, David F. Scarciglia, Sara Adams, Claire Fog Nielsen, Kristian Gram, Lone O’Gara, Fergal Front Microbiol Microbiology Despite 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. Frontiers Media S.A. 2019-09-11 /pmc/articles/PMC6749037/ /pubmed/31572336 http://dx.doi.org/10.3389/fmicb.2019.02131 Text en Copyright © 2019 Reen, Gutiérrez-Barranquero, McCarthy, Woods, Scarciglia, Adams, Fog Nielsen, Gram and O’Gara. http://creativecommons.org/licenses/by/4.0/ 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.
spellingShingle Microbiology
Reen, F. Jerry
Gutiérrez-Barranquero, José A.
McCarthy, Ronan R.
Woods, David F.
Scarciglia, Sara
Adams, Claire
Fog Nielsen, Kristian
Gram, Lone
O’Gara, Fergal
Quorum Sensing Signaling Alters Virulence Potential and Population Dynamics in Complex Microbiome-Host Interactomes
title Quorum Sensing Signaling Alters Virulence Potential and Population Dynamics in Complex Microbiome-Host Interactomes
title_full Quorum Sensing Signaling Alters Virulence Potential and Population Dynamics in Complex Microbiome-Host Interactomes
title_fullStr Quorum Sensing Signaling Alters Virulence Potential and Population Dynamics in Complex Microbiome-Host Interactomes
title_full_unstemmed Quorum Sensing Signaling Alters Virulence Potential and Population Dynamics in Complex Microbiome-Host Interactomes
title_short Quorum Sensing Signaling Alters Virulence Potential and Population Dynamics in Complex Microbiome-Host Interactomes
title_sort quorum sensing signaling alters virulence potential and population dynamics in complex microbiome-host interactomes
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6749037/
https://www.ncbi.nlm.nih.gov/pubmed/31572336
http://dx.doi.org/10.3389/fmicb.2019.02131
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