Epinephrine affects motility, and increases adhesion, biofilm and virulence of Pseudomonas aeruginosa H103

Cambronel, Mélyssa; Tortuel, Damien; Biaggini, Kelly; Maillot, Olivier; Taupin, Laure; Réhel, Karine; Rincé, Isabelle; Muller, Cécile; Hardouin, Julie; Feuilloley, Marc; Rodrigues, Sophie; Connil, Nathalie

doi:10.1038/s41598-019-56666-7

Cited by 34 publications

(22 citation statements)

References 56 publications

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“…Recently, a growing interest in the microbial responses to human-derived hormones has spread in the scientific community, mainly concerning pathogenic/opportunistic bacteria [49]. In a previous paper, we evaluated the phenotypic and proteomic modifications occurring in the probiotic E. faecium NCIMB 10415 after NE stimulation [13].…”

Section: Discussionmentioning

confidence: 99%

Serotonin Exposure Improves Stress Resistance, Aggregation, and Biofilm Formation in the Probiotic Enterococcus faecium NCIMB10415

Scardaci

Manfredi

Barberis

et al. 2021

Microbiology Research

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The role of the microbiota–gut–brain axis in maintaining a healthy status is well recognized. In this bidirectional flux, the influence of host hormones on gut bacteria is crucial. However, data on commensal/probiotics are scarce since most reports analyzed the effects of human bioactive compounds on opportunistic strains, highlighting the risk of increased pathogenicity under stimulation. The present investigation examined the modifications induced by 5HT, a tryptophan-derived molecule abundant in the intestine, on the probiotic Enterococcus faecium NCIMB10415. Specific phenotypic modifications concerning the probiotic potential and possible effects of treated bacteria on dendritic cells were explored together with the comparative soluble proteome evaluation. Increased resistance to bile salts and ampicillin in 5HT-stimulated conditions relate with overexpression of specific proteins (among which Zn-beta-lactamases, a Zn-transport protein and a protein involved in fatty acid incorporation into the membrane). Better auto-aggregating properties and biofilm-forming aptitude are consistent with enhanced QS peptide transport. Concerning interaction with the host, E. faecium NCIMB10415 enhanced dendritic cell maturation, but no significant differences were observed between 5HT-treated and untreated bacteria; meanwhile, after 5HT exposure, some moonlight proteins possibly involved in tissue adhesion were found in higher abundance. Finally, the finding in stimulated conditions of a higher abundance of VicR, a protein involved in two-component signal transduction system (VicK/R), suggests the existence of a possible surface receptor (VicK) for 5HT sensing in the strain studied. These overall data indicate that E. faecium NCIMB10415 modifies its physiology in response to 5HT by improving bacterial interactions and resistance to stressors.

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Section: Discussionmentioning

confidence: 99%

Serotonin Exposure Improves Stress Resistance, Aggregation, and Biofilm Formation in the Probiotic Enterococcus faecium NCIMB10415

Scardaci

Manfredi

Barberis

et al. 2021

Microbiology Research

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“…On the contrary, NE had less effect on biofilm formation of these bacteria. In the literature, the capacity of catecholamines to enhance biofilms has been previously observed for several Gramnegative bacteria, including E. coli O157:H7 (Bansal et al, 2007), Vibrio harveyi (Yang et al, 2014) and Pseudomonas aeruginosa (Freestone et al, 2012;Cambronel et al, 2019). Few studies have been conducted on Gram-positive bacteria.…”

Section: Discussionmentioning

confidence: 99%

Influence of Catecholamines (Epinephrine/Norepinephrine) on Biofilm Formation and Adhesion in Pathogenic and Probiotic Strains of Enterococcus faecalis

et al. 2020

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Enterococcus faecalis has controversial status due to its emerging role in nosocomial infections, while some strains with beneficial effects are used as probiotics and starter cultures in dairy industry. These bacteria can be found as resident or transient germs in the gut or on skin, where they are continually exposed to various eukaryotic molecules. In this context, the aim of our work was to evaluate the effect of the catecholamine stress hormones, epinephrine (Epi), and norepinephrine (NE) on some Enterococcus s trains. Four E. faecalis strains were included in this study: E. faecalis MMH594 and E. faecalis V583, pathogenic strains of clinical origin, E. faecalis Symbioflor 1 clone DSM 16431, a pharmaceutical probiotic, and E. faecalis OB15, a probiotic strain previously isolated from Tunisian rigouta ( Baccouri et al., 2019 ). Epi was found to modulate the formation of biofilm (biovolume and thickness) in E. faecalis , whether pathogens or probiotics. NE had less effect on biofilm formation of these bacteria. We also investigated the effect of Epi and NE on adhesion of E. faecalis to eukaryotic cells as it is the first step of colonization of the host. Epi was found to significantly enhance the adhesion of MMH594 and OB15 to Caco-2/TC7 intestinal cells and HaCaT keratinocyte cells, whereas NE significantly increased the adhesion of V583 and Symbioflor 1 DSM 16431 to Caco-2/TC7 cells, the adhesion of MMH594, Symbioflor 1 DSM 16431, and OB15 to HaCaT cells. Analysis of a putative adrenergic sensor of Epi/NE in E. faecalis , compared to QseC, the Escherichia coli adrenergic receptor, allowed the identification of VicK as the nearest protein to QseC with 29% identity and 46% similarity values. Structure modeling and molecular docking of VicK corroborated the hypothesis of possible interactions of this putative adrenergic sensor with Epi and NE, with binding energies of −4.08 and −4.49 kcal/mol, respectively. In conclusion, this study showed for the first time that stress hormones could increase biofilm formation and adhesion to eukaryotic cells in E. faecalis . Future experiments will aim to confirm by in vivo studies the role of VicK as adrenergic sensor in E. faecalis probiotic and pathogen strains. This may help to develop new strategies of antagonism/competition in the gut or skin ecological niches, and to prevent the colonization by opportunistic pathogens.

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“…Considering the gut mucosa is a milieu of neurochemicals, not solely serotonin, further studies should assess whether the effect of serotonin on C. jejuni adhesion occurs in vivo . Indeed, catecholamine neurochemicals that are present in the gut have been reported to affect bacterial adhesion ( Cambronel et al., 2019 ; Cambronel et al., 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Serotonin modulates Campylobacter jejuni physiology and in vitro interaction with the gut epithelium

et al. 2021

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Microbial endocrinology, which is the study of neurochemical-based host–microbe interaction, has demonstrated that neurochemicals affect bacterial pathogenicity. A variety of neurochemicals, including norepinephrine, were shown to enhance intestinal epithelial colonization by Campylobacter jejuni. Yet, little is known whether serotonin, an abundant neurochemical produced in the gut, affects the physiology of C. jejuni and its interaction with the host gut epithelium. Considering the avian gut produces serotonin and serves as a major reservoir of C. jejuni , we sought to investigate whether serotonin can affect C. jejuni physiology and gut epithelial colonization in vitro . We first determined the biogeographical distribution of serotonin concentrations in the serosa, mucosa, as well as the luminal contents of the broiler chicken ileum, cecum, and colon. Serotonin concentrations were greater ( P < 0.05) in the mucosa and serosa compared to the luminal content in each gut region examined. Among the ileum, colon, and cecum, the colon was found to contain the greatest concentrations of serotonin. We then investigated whether serotonin may effect changes in C. jejuni growth and motility in vitro . The C. jejuni used in this study was previously isolated from the broiler chicken ceca. Serotonin at concentrations of 1mM or below did not elicit changes in growth ( P > 0.05) or motility ( P > 0.05) of C. jejuni . Next, we utilized liquid chromatography tandem mass spectrometry to investigate whether serotonin affected the proteome of C. jejuni . Serotonin caused ( P < 0.05) the downregulation of a protein ( CJJ81176_1037 ) previously identified to be essential in C. jejuni colonization. Based on our findings, we evaluated whether serotonin would cause a functional change in C. jejuni adhesion and invasion of the HT29MTX-E12 colonic epithelial cell line. Serotonin was found to cause a reduction in adhesion ( P < 0.05) but not invasion ( P > 0.05). Together, we have identified a potential role for serotonin in modulating C. jejuni colonization in the gut in vitro . Further studies are required to understand the practical implications of these findings for the control of C. jejuni enteric colonization in vivo .

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Epinephrine affects motility, and increases adhesion, biofilm and virulence of Pseudomonas aeruginosa H103

Cited by 34 publications

References 56 publications

Serotonin Exposure Improves Stress Resistance, Aggregation, and Biofilm Formation in the Probiotic Enterococcus faecium NCIMB10415

Serotonin Exposure Improves Stress Resistance, Aggregation, and Biofilm Formation in the Probiotic Enterococcus faecium NCIMB10415

Influence of Catecholamines (Epinephrine/Norepinephrine) on Biofilm Formation and Adhesion in Pathogenic and Probiotic Strains of Enterococcus faecalis

Serotonin modulates Campylobacter jejuni physiology and in vitro interaction with the gut epithelium

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