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.
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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
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
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
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
Belay T, Sonnenfeld G (2002) Differential effects of catecholamines on in vitro growth of pathogenic bacteria. Life Sci 71(4):447–456
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
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
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
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
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
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
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
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
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
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
Kowalska K, Carr DB, Lipkowski AW (2002) Direct antimicrobial properties of substance P. Life Sci 71(7):747–750
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
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
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
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
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
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
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
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
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
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
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
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
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
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)
Silby MW, Winstanley C, Godfrey SA, Levy SB, Jackson RW (2011) Pseudomonas genomes: diverse and adaptable. FEMS Microbiol Rev 35(4):652–680
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
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
Steer HW, Colin-Jones DG (1975) Mucosal changes in gastric ulceration and their response to carbenoxolone sodium. Gut 16(8):590–597
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
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
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
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
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
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
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
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Communicated by Djamel Drider.
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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
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DOI: https://doi.org/10.1007/s00203-015-1135-y