Full Transcriptomic Response of Pseudomonas aeruginosa to an Inulin-Derived Fructooligosaccharide

Pseudomonas aeruginosa is an ubiquitous gram-negative opportunistic human pathogen which is not considered part of the human commensal gut microbiota. However, depletion of the intestinal microbiota (Dysbiosis) following antibiotic treatment facilitates the colonization of the intestinal tract by Mu...

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Main Authors: José Manuel Rubio-Gómez, Carlos Molina Santiago, Zulema Udaondo, Mireia Tena Garitaonaindia, Tino Krell, Juan-Luis Ramos, Abdelali Daddaoua
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.00202/full
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spelling doaj-7df407d49f4d4b60b72ffab77a380c342020-11-25T00:18:41ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-02-011110.3389/fmicb.2020.00202514563Full Transcriptomic Response of Pseudomonas aeruginosa to an Inulin-Derived FructooligosaccharideJosé Manuel Rubio-Gómez0Carlos Molina Santiago1Zulema Udaondo2Mireia Tena Garitaonaindia3Tino Krell4Juan-Luis Ramos5Abdelali Daddaoua6Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas, Department of Pharmacology, School of Pharmacy, University of Granada, Granada, SpainDepartment of Microbiology, Instituto de Hortofruticultura Subtropical y Mediterránea “La Mayora”, University of Málaga, Málaga, SpainDepartment of Biomedical Informatics, University of Arkansas for Medical Sciences, Little Rock, AR, United StatesDepartment of Biochemistry and Molecular Biology II, School of Pharmacy, University of Granada, Granada, SpainDepartment of Environmental Protection, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainDepartment of Environmental Protection, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainDepartment of Biochemistry and Molecular Biology II, School of Pharmacy, University of Granada, Granada, SpainPseudomonas aeruginosa is an ubiquitous gram-negative opportunistic human pathogen which is not considered part of the human commensal gut microbiota. However, depletion of the intestinal microbiota (Dysbiosis) following antibiotic treatment facilitates the colonization of the intestinal tract by Multidrug-Resistant P. aeruginosa. One possible strategy is based on the use of functional foods with prebiotic activity. The bifidogenic effect of the prebiotic inulin and its hydrolyzed form (fructooligosaccharide: FOS) is well established since they promote the growth of specific beneficial (probiotic) gut bacteria such as bifidobacteria. Previous studies of the opportunistic nosocomial pathogen Pseudomonas aeruginosa PAO1 have shown that inulin and to a greater extent FOS reduce growth and biofilm formation, which was found to be due to a decrease in motility and exotoxin secretion. However, the transcriptional basis for these phenotypic alterations remains unclear. To address this question we conducted RNA-sequence analysis. Changes in the transcript level induced by inulin and FOS were similar, but a set of transcript levels were increased in response to inulin and reduced in the presence of FOS. In the presence of inulin or FOS, 260 and 217 transcript levels, respectively, were altered compared to the control to which no polysaccharide was added. Importantly, changes in transcript levels of 57 and 83 genes were found to be specific for either inulin or FOS, respectively, indicating that both compounds trigger different changes. Gene pathway analyses of differentially expressed genes (DEG) revealed a specific FOS-mediated reduction in transcript levels of genes that participate in several canonical pathways involved in metabolism and growth, motility, biofilm formation, β-lactamase resistance, and in the modulation of type III and VI secretion systems; results that have been partially verified by real time quantitative PCR measurements. Moreover, we have identified a genomic island formed by a cluster of 15 genes, encoding uncharacterized proteins, which were repressed in the presence of FOS. The analysis of isogenic mutants has shown that genes of this genomic island encode proteins involved in growth, biofilm formation and motility. These results indicate that FOS selectively modulates bacterial pathogenicity by interfering with different signaling pathways.https://www.frontiersin.org/article/10.3389/fmicb.2020.00202/fullRNA sequencingrt-qPCRadhesiondevelopmental processmolecular transducerpathogenicity
collection DOAJ
language English
format Article
sources DOAJ
author José Manuel Rubio-Gómez
Carlos Molina Santiago
Zulema Udaondo
Mireia Tena Garitaonaindia
Tino Krell
Juan-Luis Ramos
Abdelali Daddaoua
spellingShingle José Manuel Rubio-Gómez
Carlos Molina Santiago
Zulema Udaondo
Mireia Tena Garitaonaindia
Tino Krell
Juan-Luis Ramos
Abdelali Daddaoua
Full Transcriptomic Response of Pseudomonas aeruginosa to an Inulin-Derived Fructooligosaccharide
Frontiers in Microbiology
RNA sequencing
rt-qPCR
adhesion
developmental process
molecular transducer
pathogenicity
author_facet José Manuel Rubio-Gómez
Carlos Molina Santiago
Zulema Udaondo
Mireia Tena Garitaonaindia
Tino Krell
Juan-Luis Ramos
Abdelali Daddaoua
author_sort José Manuel Rubio-Gómez
title Full Transcriptomic Response of Pseudomonas aeruginosa to an Inulin-Derived Fructooligosaccharide
title_short Full Transcriptomic Response of Pseudomonas aeruginosa to an Inulin-Derived Fructooligosaccharide
title_full Full Transcriptomic Response of Pseudomonas aeruginosa to an Inulin-Derived Fructooligosaccharide
title_fullStr Full Transcriptomic Response of Pseudomonas aeruginosa to an Inulin-Derived Fructooligosaccharide
title_full_unstemmed Full Transcriptomic Response of Pseudomonas aeruginosa to an Inulin-Derived Fructooligosaccharide
title_sort full transcriptomic response of pseudomonas aeruginosa to an inulin-derived fructooligosaccharide
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2020-02-01
description Pseudomonas aeruginosa is an ubiquitous gram-negative opportunistic human pathogen which is not considered part of the human commensal gut microbiota. However, depletion of the intestinal microbiota (Dysbiosis) following antibiotic treatment facilitates the colonization of the intestinal tract by Multidrug-Resistant P. aeruginosa. One possible strategy is based on the use of functional foods with prebiotic activity. The bifidogenic effect of the prebiotic inulin and its hydrolyzed form (fructooligosaccharide: FOS) is well established since they promote the growth of specific beneficial (probiotic) gut bacteria such as bifidobacteria. Previous studies of the opportunistic nosocomial pathogen Pseudomonas aeruginosa PAO1 have shown that inulin and to a greater extent FOS reduce growth and biofilm formation, which was found to be due to a decrease in motility and exotoxin secretion. However, the transcriptional basis for these phenotypic alterations remains unclear. To address this question we conducted RNA-sequence analysis. Changes in the transcript level induced by inulin and FOS were similar, but a set of transcript levels were increased in response to inulin and reduced in the presence of FOS. In the presence of inulin or FOS, 260 and 217 transcript levels, respectively, were altered compared to the control to which no polysaccharide was added. Importantly, changes in transcript levels of 57 and 83 genes were found to be specific for either inulin or FOS, respectively, indicating that both compounds trigger different changes. Gene pathway analyses of differentially expressed genes (DEG) revealed a specific FOS-mediated reduction in transcript levels of genes that participate in several canonical pathways involved in metabolism and growth, motility, biofilm formation, β-lactamase resistance, and in the modulation of type III and VI secretion systems; results that have been partially verified by real time quantitative PCR measurements. Moreover, we have identified a genomic island formed by a cluster of 15 genes, encoding uncharacterized proteins, which were repressed in the presence of FOS. The analysis of isogenic mutants has shown that genes of this genomic island encode proteins involved in growth, biofilm formation and motility. These results indicate that FOS selectively modulates bacterial pathogenicity by interfering with different signaling pathways.
topic RNA sequencing
rt-qPCR
adhesion
developmental process
molecular transducer
pathogenicity
url https://www.frontiersin.org/article/10.3389/fmicb.2020.00202/full
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