Serotonin Activates Bacterial Quorum Sensing and Enhances the Virulence of Pseudomonas aeruginosa in the Host

Bacteria in humans play an important role in health and disease. Considerable emphasis has been placed in understanding the role of bacteria in host-microbiome interkingdom communication. Here we show that serotonin, responsible for mood in the brain and motility in the gut, can also act as a bacter...

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Published in:	EBioMedicine Vol. 9; no. C; pp. 161 - 169
Main Authors:	Knecht, Leslie D., O'Connor, Gregory, Mittal, Rahul, Liu, Xue Z., Daftarian, Pirouz, Deo, Sapna K., Daunert, Sylvia
Format:	Journal Article
Language:	English
Published:	Netherlands Elsevier B.V 01.07.2016 Elsevier
Subjects:	Advanced Basic Science Animals Bacterial Proteins - metabolism Catalase - metabolism Cytokines - analysis Female Host-microbiome interactions Injections, Intraperitoneal Interkingdom signaling molecule Internal Medicine Intestines - metabolism Intestines - microbiology Intestines - pathology Las pathway Malondialdehyde - metabolism Mice Mice, Inbred C57BL Microscopy, Electron, Scanning N-acyl homoserine lactone Peptide Hydrolases - metabolism Peroxidase - metabolism Phenotype Pregnancy Pseudomonas aeruginosa Pseudomonas aeruginosa - enzymology Pseudomonas aeruginosa - metabolism Pseudomonas aeruginosa - physiology Quorum sensing Quorum Sensing - drug effects Research Paper Serotonin Serotonin - pharmacology Virulence - drug effects Serotonin Las pathway Pseudomonas aeruginosa Host-microbiome interactions Quorum sensing Interkingdom signaling molecule N-acyl homoserine lactone
ISSN:	2352-3964, 2352-3964
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Abstract	Bacteria in humans play an important role in health and disease. Considerable emphasis has been placed in understanding the role of bacteria in host-microbiome interkingdom communication. Here we show that serotonin, responsible for mood in the brain and motility in the gut, can also act as a bacterial signaling molecule for pathogenic bacteria. Specifically, we found that serotonin acts as an interkingdom signaling molecule via quorum sensing and that it stimulates the production of bacterial virulence factors and increases biofilm formation in vitro and in vivo in a novel mouse infection model. This discovery points out at roles of serotonin both in bacteria and humans, and at phenotypic implications not only manifested in mood behavior but also in infection processes in the host. Thus, regulating serotonin concentrations in the gut may provide with paradigm shifting therapeutic approaches. •Serotonin can act as a bacterial quorum sensing molecule through the LasR quorum sensing pathway.•Serotonin stimulates quorum sensing-dependent virulence factor and biofilm production in Pseudomonas aeruginosa.•Serotonin exacerbates Pseudomonas aeruginosa infection in vivo. Bacteria play many roles in human health and disease, thus investigating host-microbiome communication is of great importance. To this end, our research demonstrates that serotonin, a neurotransmitter responsible for mood in the brain and motility in the gut, can act as a bacterial communication molecule for pathogenic bacteria, specifically Pseudomonas aeruginosa. Serotonin increases Pseudomonas virulence factor and biofilm production in vitro and enhances virulence in infected mice. These findings are beneficial in understanding the impact of the microbiome on human health and may open the door for novel treatments for human disease.
AbstractList	Bacteria in humans play an important role in health and disease. Considerable emphasis has been placed in understanding the role of bacteria in host-microbiome interkingdom communication. Here we show that serotonin, responsible for mood in the brain and motility in the gut, can also act as a bacterial signaling molecule for pathogenic bacteria. Specifically, we found that serotonin acts as an interkingdom signaling molecule via quorum sensing and that it stimulates the production of bacterial virulence factors and increases biofilm formation in vitro and in vivo in a novel mouse infection model. This discovery points out at roles of serotonin both in bacteria and humans, and at phenotypic implications not only manifested in mood behavior but also in infection processes in the host. Thus, regulating serotonin concentrations in the gut may provide with paradigm shifting therapeutic approaches. AbstractBacteria in humans play an important role in health and disease. Considerable emphasis has been placed in understanding the role of bacteria in host-microbiome interkingdom communication. Here we show that serotonin, responsible for mood in the brain and motility in the gut, can also act as a bacterial signaling molecule for pathogenic bacteria. Specifically, we found that serotonin acts as an interkingdom signaling molecule via quorum sensing and that it stimulates the production of bacterial virulence factors and increases biofilm formation in vitro and in vivo in a novel mouse infection model. This discovery points out at roles of serotonin both in bacteria and humans, and at phenotypic implications not only manifested in mood behavior but also in infection processes in the host. Thus, regulating serotonin concentrations in the gut may provide with paradigm shifting therapeutic approaches. Bacteria in humans play an important role in health and disease. Considerable emphasis has been placed in understanding the role of bacteria in host-microbiome interkingdom communication. Here we show that serotonin, responsible for mood in the brain and motility in the gut, can also act as a bacterial signaling molecule for pathogenic bacteria. Specifically, we found that serotonin acts as an interkingdom signaling molecule via quorum sensing and that it stimulates the production of bacterial virulence factors and increases biofilm formation in vitro and in vivo in a novel mouse infection model. This discovery points out at roles of serotonin both in bacteria and humans, and at phenotypic implications not only manifested in mood behavior but also in infection processes in the host. Thus, regulating serotonin concentrations in the gut may provide with paradigm shifting therapeutic approaches. • Serotonin can act as a bacterial quorum sensing molecule through the LasR quorum sensing pathway. • Serotonin stimulates quorum sensing-dependent virulence factor and biofilm production in Pseudomonas aeruginosa. • Serotonin exacerbates Pseudomonas aeruginosa infection in vivo. Bacteria play many roles in human health and disease, thus investigating host-microbiome communication is of great importance. To this end, our research demonstrates that serotonin, a neurotransmitter responsible for mood in the brain and motility in the gut, can act as a bacterial communication molecule for pathogenic bacteria, specifically Pseudomonas aeruginosa. Serotonin increases Pseudomonas virulence factor and biofilm production in vitro and enhances virulence in infected mice. These findings are beneficial in understanding the impact of the microbiome on human health and may open the door for novel treatments for human disease. Bacteria in humans play an important role in health and disease. Considerable emphasis has been placed in understanding the role of bacteria in host-microbiome interkingdom communication. Here we show that serotonin, responsible for mood in the brain and motility in the gut, can also act as a bacterial signaling molecule for pathogenic bacteria. Specifically, we found that serotonin acts as an interkingdom signaling molecule via quorum sensing and that it stimulates the production of bacterial virulence factors and increases biofilm formation in vitro and in vivo in a novel mouse infection model. This discovery points out at roles of serotonin both in bacteria and humans, and at phenotypic implications not only manifested in mood behavior but also in infection processes in the host. Thus, regulating serotonin concentrations in the gut may provide with paradigm shifting therapeutic approaches. •Serotonin can act as a bacterial quorum sensing molecule through the LasR quorum sensing pathway.•Serotonin stimulates quorum sensing-dependent virulence factor and biofilm production in Pseudomonas aeruginosa.•Serotonin exacerbates Pseudomonas aeruginosa infection in vivo. Bacteria play many roles in human health and disease, thus investigating host-microbiome communication is of great importance. To this end, our research demonstrates that serotonin, a neurotransmitter responsible for mood in the brain and motility in the gut, can act as a bacterial communication molecule for pathogenic bacteria, specifically Pseudomonas aeruginosa. Serotonin increases Pseudomonas virulence factor and biofilm production in vitro and enhances virulence in infected mice. These findings are beneficial in understanding the impact of the microbiome on human health and may open the door for novel treatments for human disease. Bacteria in humans play an important role in health and disease. Considerable emphasis has been placed in understanding the role of bacteria in host-microbiome interkingdom communication. Here we show that serotonin, responsible for mood in the brain and motility in the gut, can also act as a bacterial signaling molecule for pathogenic bacteria. Specifically, we found that serotonin acts as an interkingdom signaling molecule via quorum sensing and that it stimulates the production of bacterial virulence factors and increases biofilm formation in vitro and in vivo in a novel mouse infection model. This discovery points out at roles of serotonin both in bacteria and humans, and at phenotypic implications not only manifested in mood behavior but also in infection processes in the host. Thus, regulating serotonin concentrations in the gut may provide with paradigm shifting therapeutic approaches.Bacteria in humans play an important role in health and disease. Considerable emphasis has been placed in understanding the role of bacteria in host-microbiome interkingdom communication. Here we show that serotonin, responsible for mood in the brain and motility in the gut, can also act as a bacterial signaling molecule for pathogenic bacteria. Specifically, we found that serotonin acts as an interkingdom signaling molecule via quorum sensing and that it stimulates the production of bacterial virulence factors and increases biofilm formation in vitro and in vivo in a novel mouse infection model. This discovery points out at roles of serotonin both in bacteria and humans, and at phenotypic implications not only manifested in mood behavior but also in infection processes in the host. Thus, regulating serotonin concentrations in the gut may provide with paradigm shifting therapeutic approaches.
Author	Deo, Sapna K. Liu, Xue Z. Knecht, Leslie D. O'Connor, Gregory Mittal, Rahul Daftarian, Pirouz Daunert, Sylvia
AuthorAffiliation	c Department of Otolaryngology, University of Miami, Miller School of Medicine, Miami, FL 33136, United States a Department of Biochemistry and Molecular Biology, University of Miami, Miller School of Medicine, Miami, FL 33136, United States b Department of Chemistry, University of Miami, Miami, FL 33146, United States
AuthorAffiliation_xml	– name: c Department of Otolaryngology, University of Miami, Miller School of Medicine, Miami, FL 33136, United States – name: b Department of Chemistry, University of Miami, Miami, FL 33146, United States – name: a Department of Biochemistry and Molecular Biology, University of Miami, Miller School of Medicine, Miami, FL 33136, United States
Author_xml	– sequence: 1 givenname: Leslie D. surname: Knecht fullname: Knecht, Leslie D. organization: Department of Biochemistry and Molecular Biology, University of Miami, Miller School of Medicine, Miami, FL 33136, United States – sequence: 2 givenname: Gregory surname: O'Connor fullname: O'Connor, Gregory organization: Department of Biochemistry and Molecular Biology, University of Miami, Miller School of Medicine, Miami, FL 33136, United States – sequence: 3 givenname: Rahul surname: Mittal fullname: Mittal, Rahul organization: Department of Otolaryngology, University of Miami, Miller School of Medicine, Miami, FL 33136, United States – sequence: 4 givenname: Xue Z. surname: Liu fullname: Liu, Xue Z. organization: Department of Otolaryngology, University of Miami, Miller School of Medicine, Miami, FL 33136, United States – sequence: 5 givenname: Pirouz surname: Daftarian fullname: Daftarian, Pirouz organization: Department of Biochemistry and Molecular Biology, University of Miami, Miller School of Medicine, Miami, FL 33136, United States – sequence: 6 givenname: Sapna K. surname: Deo fullname: Deo, Sapna K. organization: Department of Biochemistry and Molecular Biology, University of Miami, Miller School of Medicine, Miami, FL 33136, United States – sequence: 7 givenname: Sylvia surname: Daunert fullname: Daunert, Sylvia email: sdaunert@med.miami.edu organization: Department of Biochemistry and Molecular Biology, University of Miami, Miller School of Medicine, Miami, FL 33136, United States
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/27333040$$D View this record in MEDLINE/PubMed
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Keywords	Serotonin Las pathway Pseudomonas aeruginosa Host-microbiome interactions Quorum sensing Interkingdom signaling molecule N-acyl homoserine lactone
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Snippet	Bacteria in humans play an important role in health and disease. Considerable emphasis has been placed in understanding the role of bacteria in host-microbiome... AbstractBacteria in humans play an important role in health and disease. Considerable emphasis has been placed in understanding the role of bacteria in...
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SubjectTerms	Advanced Basic Science Animals Bacterial Proteins - metabolism Catalase - metabolism Cytokines - analysis Female Host-microbiome interactions Injections, Intraperitoneal Interkingdom signaling molecule Internal Medicine Intestines - metabolism Intestines - microbiology Intestines - pathology Las pathway Malondialdehyde - metabolism Mice Mice, Inbred C57BL Microscopy, Electron, Scanning N-acyl homoserine lactone Peptide Hydrolases - metabolism Peroxidase - metabolism Phenotype Pregnancy Pseudomonas aeruginosa Pseudomonas aeruginosa - enzymology Pseudomonas aeruginosa - metabolism Pseudomonas aeruginosa - physiology Quorum sensing Quorum Sensing - drug effects Research Paper Serotonin Serotonin - pharmacology Virulence - drug effects
Title	Serotonin Activates Bacterial Quorum Sensing and Enhances the Virulence of Pseudomonas aeruginosa in the Host
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