Skip to main content
Log in

The pathogenic potential of Pseudomonas fluorescens MFN1032 on enterocytes can be modulated by serotonin, substance P and epinephrine

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Pseudomonas fluorescens is a commensal bacterium present at low level in the human digestive tract that has also been reported in many clinical samples (blood, urinary tract, skin, lung, etc.) and sometimes associated with acute opportunistic infections. It has recently been found that the human β-defensin-2 can enhance the pathogenic potential of P. fluorescens. In this study, we evaluated the effect of other intestinal molecules (5HT, SP and Epi) on growth and virulence of the clinical strain P. fluorescens MFN1032. We found that P. fluorescens MFN1032 growth was not mainly affected by these factors, but several modifications in the virulence behavior of this bacterium were observed. 5HT, SP and Epi were able to modulate the motility of P. fluorescens MFN1032. 5HT and SP had an effect on pyoverdin production and IL-8 secretion, respectively. Infection of Caco-2/TC7 cells with P. fluorescens MFN1032 pretreated by SP or Epi enhanced the permeability of the monolayers and led to a partial delocalization of F-actin to the cytoplasm. These findings show that some intestinal molecules can modulate the pathogenic potential of P. fluorescens MFN1032. We can hypothesize that this dialogue between the host and the human gut microbiota may participate in health and disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alnabhani Z, Montcuquet N, Biaggini K, Dussaillant M, Roy M, Ogier-Denis E, Madi A, Jallane A, Feuilloley M, Hugot JP, Connil N, Barreau F (2015) Pseudomonas fluorescens alters the intestinal barrier function by modulating IL-1β expression through hematopoietic NOD2 signaling. Inflamm Bowel Dis 21(3):543–555

    Article  PubMed  Google Scholar 

  • Alsohim AS, Taylor TB, Barrett GA, Gallie J, Zhang XX, Altamirano-Junqueira AE, Johnson LJ, Rainey PB, Jackson RW (2014) The biosurfactant viscosin produced by Pseudomonas fluorescens SBW25 aids spreading motility and plant growth promotion. Environ Microbiol 16(7):2267–2281

    Article  CAS  PubMed  Google Scholar 

  • Alverdy J, Holbrook C, Rocha F, Seiden L, Wu RL, Musch M, Chang E, Ohman D, Suh S (2000) Gut-derived sepsis occurs when the right pathogen with the right virulence genes meets the right host: evidence for in vivo virulence expression in Pseudomonas aeruginosa. Ann Surg 232(4):480–489

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Anuchin AM, Chuvelev DI, Kirovskaya TA, Oleskin AV (2008) Effects of monoamine neuromediators on the growth-related variables of Escherichia coli K-12. Mikrobiologiia 77(6):674–680

  • Bansal T, Englert D, Lee J, Hegde M, Wood TK, Jayaraman A (2007) Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression. Infect Immun 75(9):4597–4607

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Belay T, Sonnenfeld G (2002) Differential effects of catecholamines on in vitro growth of pathogenic bacteria. Life Sci 71(4):447–456

    Article  CAS  PubMed  Google Scholar 

  • Belay T, Aviles H, Vance M, Fountain K, Sonnenfeld G (2003) Catecholamines and in vitro growth of pathogenic bacteria: enhancement of growth varies greatly among bacterial species. Life Sci 73(12):1527–1535

    Article  CAS  PubMed  Google Scholar 

  • Chapalain A, Rossignol G, Lesouhaitier O, Merieau A, Gruffaz C, Guerillon J, Meyer JM, Orange N, Feuilloley MG (2008) Comparative study of 7 fluorescent pseudomonad clinical isolates. Can J Microbiol 54:19–27

    Article  CAS  PubMed  Google Scholar 

  • Clarke MB, Hughes DT, Zhu C, Boedeker EC, Sperandio V (2006) The QseC sensor kinase: a bacterial adrenergic receptor. Proc Natl Acad Sci USA 103(27):10420–10425

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cogan TA, Thomas AO, Rees LE, Taylor AH, Jepson MA, Williams PH, Ketley J, Humphrey TJ (2007) Norepinephrine increases the pathogenic potential of Campylobacter jejuni. Gut 56(8):1060–1065

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dagorn A, Chapalain A, Mijouin L, Hillion M, Duclairoir-Poc C, Chevalier S, Taupin L, Orange N, Feuilloley MG (2013) Effect of GABA, a bacterial metabolite, on Pseudomonas fluorescens surface properties and cytotoxicity. Int J Mol Sci 14(6):12186–12204

    Article  PubMed Central  PubMed  Google Scholar 

  • Dalwadi H, Wei B, Kronenberg M, Sutton CL, Braun J (2001) The Crohn’s disease-associated bacterial protein I2 is a novel enteric t cell superantigen. Immunity 15(1):149–158

    Article  CAS  PubMed  Google Scholar 

  • Dickson RP, Erb-Downward JR, Freeman CM, Walker N, Scales BS, Beck JM, Martinez FJ, Curtis JL, Lama VN, Huffnagle GB (2014) Changes in the lung microbiome following lung transplantation include the emergence of two distinct pseudomonas species with distinct clinical associations. PLoS ONE 9(5):e97214

    Article  PubMed Central  PubMed  Google Scholar 

  • Domínguez-Bello MG, Reyes N, Teppa-Garrán A, Romero R (2000) Interference of Pseudomonas strains in the identification of Helicobacter pylori. J Clin Microbiol 38(2):937

    PubMed Central  PubMed  Google Scholar 

  • Donnarumma G, Buommino E, Fusco A, Paoletti I, Auricchio L, Tufano MA (2010) Effect of temperature on the shift of Pseudomonas fluorescens from an environmental microorganism to a potential human pathogen. Int J Immunopathol Pharmacol 23(1):227–234

    CAS  PubMed  Google Scholar 

  • Hansen CJ, Burnell KK, Brogden KA (2006) Antimicrobial activity of Substance P and Neuropeptide Y against laboratory strains of bacteria and oral microorganisms. J Neuroimmunol 177(1–2):215–218

    Article  CAS  PubMed  Google Scholar 

  • Kowalska K, Carr DB, Lipkowski AW (2002) Direct antimicrobial properties of substance P. Life Sci 71(7):747–750

    Article  CAS  PubMed  Google Scholar 

  • Lesouhaitier O, Veron W, Chapalain A, Madi A, Blier AS, Dagorn A, Connil N, Chevalier S, Orange N, Feuilloley M (2009) Gram-negative bacterial sensors for eukaryotic signal molecules. Sensors 9(9):6967–6990

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li W, Lyte M, Freestone PP, Ajmal A, Colmer-Hamood JA, Hamood AN (2009) Norepinephrine represses the expression of toxA and the siderophore genes in Pseudomonas aeruginosa. FEMS Microbiol Lett 299(1):100–109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Long TM, Nisa S, Donnenberg MS, Hassel BA (2014) Enteropathogenic Escherichia coli inhibits type I interferon- and RNase L-mediated host defense to disrupt intestinal epithelial cell barrier function. Infect Immun 82(7):2802–2814

    Article  PubMed Central  PubMed  Google Scholar 

  • Madi A, Lakhdari O, Blottière HM, Guyard-Nicodème M, Le Roux K, Groboillot A, Svinareff P, Doré J, Orange N, Feuilloley MG, Connil N (2010) The clinical Pseudomonas fluorescens MFN1032 strain exerts a cytotoxic effect on epithelial intestinal cells and induces interleukin-8 via the AP-1 signaling pathway. BMC Microbiol 10:215

    Article  PubMed Central  PubMed  Google Scholar 

  • Madi A, Alnabhani Z, Leneveu C, Mijouin L, Feuilloley M, Connil N (2013) Pseudomonas fluorescens can induce and divert the human β-defensin-2 secretion in intestinal epithelial cells to enhance its virulence. Arch Microbiol 195(3):189–195

    Article  CAS  PubMed  Google Scholar 

  • Meyer JM, Neely A, Stintzi A, Georges C, Holder IA (1996) Pyoverdin is essential for virulence of Pseudomonas aeruginosa. Infect Immun 64(2):518–523

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mijouin L, Hillion M, Ramdani Y, Jaouen T, Duclairoir-Poc C, Follet-Gueye ML, Lati E, Yvergnaux F, Driouich A, Lefeuvre L, Farmer C, Misery L, Feuilloley MG (2013) Effects of a skin neuropeptide (substance p) on cutaneous microflora. PLoS ONE 8(11):e78773

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moreira CG, Weinshenker D, Sperandio V (2010) QseC mediates Salmonella enterica serovar typhimurium virulence in vitro and in vivo. Infect Immun 78(3):914–926

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Okumura CY, Nizet V (2014) Subterfuge and sabotage: evasion of host innate defenses by invasive gram-positive bacterial pathogens. Annu Rev Microbiol 68:439–458

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Patel SK, Pratap CB, Verma AK, Jain AK, Dixit VK, Nath G (2013) Pseudomonas fluorescens-like bacteria from the stomach: a microbiological and molecular study. World J Gastroenterol 19(7):1056–1067

    Article  PubMed Central  PubMed  Google Scholar 

  • Phalipon A, Sansonetti PJ (2007) Shigella’s ways of manipulating the host intestinal innate and adaptive immune system: a tool box for survival? Immunol Cell Biol 85(2):119–129

    Article  CAS  PubMed  Google Scholar 

  • Rossignol G, Merieau A, Guerillon J, Veron W, Lesouhaitier O, Feuilloley MG, Orange N (2008) Involvement of a phospholipase C in the hemolytic activity of a clinical strain of Pseudomonas fluorescens. BMC Microbiol 8:189

    Article  PubMed Central  PubMed  Google Scholar 

  • Rossignol G, Sperandio D, Guerillon J, Duclairoir Poc C, Soum-Soutera E, Orange N, Feuilloley MG, Merieau A (2009) Phenotypic variation in the Pseudomonas fluorescens clinical strain MFN1032. Res Microbiol 160(5):337–344

    Article  CAS  PubMed  Google Scholar 

  • Scales BS, Dickson RP, LiPuma JJ, Huffnagle GB (2014) Microbiology, genomics, and clinical significance of the Pseudomonas fluorescens species complex, an unappreciated colonizer of humans. Clin Microbiol Rev 27(4):927–948 (Review)

    Article  CAS  PubMed  Google Scholar 

  • Silby MW, Winstanley C, Godfrey SA, Levy SB, Jackson RW (2011) Pseudomonas genomes: diverse and adaptable. FEMS Microbiol Rev 35(4):652–680

    Article  CAS  PubMed  Google Scholar 

  • Sperandio D, Rossignol G, Guerillon J, Connil N, Orange N, Feuilloley MG, Merieau A (2010) Cell-associated hemolysis activity in the clinical strain of Pseudomonas fluorescens MFN1032. BMC Microbiol 10:124

    Article  PubMed Central  PubMed  Google Scholar 

  • Sperandio D, Decoin V, Latour X, Mijouin L, Hillion M, Feuilloley MG, Orange N, Merieau A (2012) Virulence of the Pseudomonas fluorescens clinical strain MFN1032 towards Dictyostelium discoideum and macrophages in relation with type III secretion system. BMC Microbiol 12:223

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Steer HW, Colin-Jones DG (1975) Mucosal changes in gastric ulceration and their response to carbenoxolone sodium. Gut 16(8):590–597

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stintzi A, Johnson Z, Stonehouse M, Ochsner U, Meyer JM, Vasil ML, Poole K (1999) The pvc gene cluster of Pseudomonas aeruginosa: role in synthesis of the pyoverdine chromophore and regulation by PtxR and PvdS. J Bacteriol 181(13):4118–4124

    PubMed Central  CAS  PubMed  Google Scholar 

  • Strakhovskaia MG, Ivanova EV, Fraĭnkin GI (1993) Stimulatory effect of serotonin on the growth of the yeast Candida guilliermondii and the bacterium Streptococcus faecalis. Mikrobiologiia 62(1):46–49

    CAS  PubMed  Google Scholar 

  • Sutton CL, Kim J, Yamane A, Dalwadi H, Wei B, Landers C, Targan SR, Braun J (2000) Identification of a novel bacterial sequence associated with Crohn’s disease. Gastroenterology 119(1):23–31

    Article  CAS  PubMed  Google Scholar 

  • Tattoli I, Sorbara MT, Yang C, Tooze SA, Philpott DJ, Girardin SE (2013) Listeria phospholipases subvert host autophagic defenses by stalling pre-autophagosomal structures. EMBO J 32(23):3066–3078

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Veron W, Orange N, Feuilloley MG, Lesouhaitier O (2008) Natriuretic peptides modify Pseudomonas fluorescens cytotoxicity by regulating cyclic nucleotides and modifying LPS structure. BMC Microbiol 8:114

    Article  PubMed Central  PubMed  Google Scholar 

  • Visca P, Leoni L, Wilson MJ, Lamont IL (2002) Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol Microbiol 45(5):1177–1190

    Article  CAS  PubMed  Google Scholar 

  • Wei B, Huang T, Dalwadi H, Sutton CL, Bruckner D (2002) Braun J (2002) Pseudomonas fluorescens encodes the Crohn’s disease-associated I2 sequence and T-cell superantigen. Infect Immun 70(12):6567–6575

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nathalie Connil.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Djamel Drider.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Biaggini, K., Barbey, C., Borrel, V. et al. The pathogenic potential of Pseudomonas fluorescens MFN1032 on enterocytes can be modulated by serotonin, substance P and epinephrine. Arch Microbiol 197, 983–990 (2015). https://doi.org/10.1007/s00203-015-1135-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-015-1135-y

Keywords

Navigation