Archives of Microbiology

, Volume 197, Issue 8, pp 983–990 | Cite as

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

  • Kelly Biaggini
  • Corinne Barbey
  • Valérie Borrel
  • Marc Feuilloley
  • Pierre Déchelotte
  • Nathalie Connil
Original Paper

Abstract

Pseudomonasfluorescens 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.

Keywords

Serotonin Substance P Epinephrine Pseudomonas fluorescens Virulence 

Introduction

Pseudomonas is a large genus, currently comprised of more than 100 species with remarkable metabolic and physiologic versatility, enabling them to adapt and colonize diverse ecological niches (Silby et al. 2011). The two best characterized Pseudomonas species are Pseudomonas aeruginosa and Pseudomonas fluorescens. P. aeruginosa is one of the most common opportunistic pathogens that are present at clinically undetectable levels in the normal gastrointestinal tract (Alverdy et al. 2000). P. fluorescens is often considered as a plant-growth-promoting rhizobacterium (Alsohim et al. 2014), but is also present in the human gut as a low level commensal (Wei et al. 2002). Interestingly, a highly specific antigen of P. fluorescens, designated as I2, was detected in the serum of 54 % of the patients suffering from Crohn’s disease (Sutton et al. 2000), and a correlation between the severity of the pathology and the level of the circulating I2 antigen has been demonstrated (Dalwadi et al. 2001). Recently, a P. fluorescens-like bacterium has been isolated from the human stomach (Patel et al. 2013) and the authors estimated that P. fluorescens may be as common as Helicobacter pylori in the gastrointestinal tract. The presence of Pseudomonas spp. in 80 % of antral biopsies has already been reported since 1975 (Steer and Colin-Jones 1975), and it has been suggested later that Pseudomonas strains may interfere with the identification of H. pylori (Domínguez-Bello et al. 2000). In the last few years, the isolation of P. fluorescens as the causative agent of nosocomial infections has rapidly increased (Donnarumma et al. 2010; Scales et al. 2014). This bacterium is also commonly isolated from respiratory specimens following lung transplantation (Dickson et al. 2014). Some clinical strains of P. fluorescens such as MFN1032 are adapted to the human physiological temperature (Chapalain et al. 2008), show various pathogenic potential (Rossignol et al. 2008, 2009; Sperandio et al. 2010, 2012) and trigger a specific inflammatory response in enterocytes (Madi et al. 2010). In fact, we also found recently that P. fluorescens could alter the intestinal barrier function by modulating IL-1β expression through hematopoietic NOD2 signaling (Alnabhani et al. 2015).

In the host, bacteria are exposed to various innate defense mechanisms, but many pathogenic germs, like Shigella, enteropathogenic Escherichia coli, Listeria, Staphylococcus or Streptococcus, are able to escape or interfere with these protection systems (Phalipon and Sansonetti. 2007; Tattoli et al. 2013; Long et al. 2014; Okumura and Nizet. 2014). We have previously found that P. fluorescens can induce and divert the human β-defensin-2 secretion in intestinal epithelial cells, leading to an increase in virulence (Madi et al. 2013). However, the enteric system, which is sometimes designated as the second brain, releases also a multitude of neurotransmitters and neurohormones, and the impact of these enteroendocrine molecules on P. fluorescens remains largely unknown.

In the present work, we investigated the effect of serotonin (5HT), substance P (SP) and epinephrine (Epi) on the growth, motility and virulence of the clinical strain P. fluorescens MFN1032.

Materials and methods

Bacterial strain

Pseudomonas fluorescens MFN1032 was collected from a pulmonary tract infection in a hospital of Haute-Normandie (France; Chapalain et al. 2008) and routinely cultivated at 28 °C, in ordinary nutrient broth (ONB; Merck, Darmstadt, Germany).

Bacterial growth with 5HT, SP and Epi

Overnight cultures of P. fluorescens MFN1032 were diluted in ONB to a final optical density (OD) of 0.08 at 600 nm. 5HT, SP or Epi were added to a final concentration of 10−3 or 10−6 M. Bacteria were then grown for 24 h with a Bioscreen spectrophotometer using the following parameters: shaking, reading every 30 min, temperature of 28 °C. Each culture was grown in triplicate, and the experiment was repeated three times.

Swarming and swimming motility assays

To test on motility, a sterile needle was used to lightly touch bacterial cultures and spotted gently in the middle of a swarm plate (Luria–Bertani Broth, 0.6 % bacteriological agar) or a swim plate (Luria–Bertani Broth, 0.3 % bacteriological agar). The plates were incubated at 28 °C, and the migration of bacteria was measured after 24 h from the point of inoculation (observed as a turbid zone in centimeters).

Production of pyoverdin

Pyoverdin production of P. fluorescens MFN1032 was determined after 48 h of growth in Bacto Casamino Acids medium (CAA). The results were expressed as the OD400 nm/OD600 nm ratio of the supernatant after removal of the bacteria by centrifugation (5 min, 10,000g) as previously described (Dagorn et al. 2013).

Caco-2/TC7 cells culture

The human colon adenocarcinoma cell line Caco-2/TC7 was used between passages 40–60. Cells were grown in Dulbecco’s modified Eagle’s medium (DMEM, Invitrogen) supplemented with 15 % heat-inactivated fetal calf serum (FCS), 2 mM of l-glutamine, 100 U ml each of penicillin and streptomycin and 1 % of nonessential amino acids. The cells were seeded and cultivated at 37 °C in 5 % CO2–95 % air atmosphere, in 24-well tissue culture plates until confluence for cytotoxicity assay and quantification of IL-8; and on inserts (6.4 mm diameter, 3 μm pore size, Falcon) until full differentiation (21 days) for transepithelial resistance measurements (TER) and actin staining.

Bacterial treatment with 5HT, SP or Epi and infection of Caco-2/TC7 cells

5HT, SP or Epi (10−6 M) were added to the cultures of P. fluorescens MFN1032 at the beginning of the exponential growth phase. After 4 h of exposition to these neuroendocrine factors, bacteria were collected by centrifugation for 5 min at 8000g, rinsed to remove any trace of the molecules and resuspended in DMEM without antibiotics and serum. Confluent or differentiated Caco-2/TC7 cells grown in 24-well plates or insert were then infected with control or treated bacteria at a MOI (multiplicity of infection) of 100:1 and incubated overnight at 37 °C in 5 % CO2.

Cytotoxicity assay and quantification of IL-8

Supernatants from Caco-2/TC7 undifferentiated monolayers were collected after 18 h of infection. The concentration of lactate dehydrogenase (LDH), a cytoplasmic enzyme released upon cell death, was determined using the Cytotox 96 enzymatic assay (Promega, France). Total LDH release (100 % dead cells) was obtained by exposing Caco-2/TC7 cells to Triton X100 (0.9 %) as recommended by the manufacturer’s instructions. IL-8 cytokine secretion was measured using ELISA Quantikine kit (R&D Systems, France).

Transepithelial resistance measurements

The transepithelial resistance (TER) of differentiated Caco-2/TC7 monolayers was measured after 18 h of bacterial infection, using the Millicell Electrical Resistance System (Millipore Corp, Bedford, MA). TER values are expressed as percentages of the initial level of the TER (baseline) measured for each individual cell monolayer in the inserts at the onset of the experiment.

Actin staining

At the end of infection, differentiated Caco-2/TC7 monolayers were washed with PBS, fixed for 10 min with 3.7 % paraformaldehyde and permeabilized for 5 min with 0.2 % Triton X100 at room temperature. The cells were then incubated with 1 % bovine serum albumin in PBS for 10 min, and the apical F-actin cytoskeleton was stained with Alexa-488 phalloidin (1 U/insert) for 45 min at room temperature. Following three washes in PBS, cell monolayers were examined using a confocal laser scanning microscope (Zeiss, LSM710) equipped with an argon laser for 488 nm excitation of Alexa-488. An oil-immersion objective lens (X63) was used, and imaging parameters standardized to allow direct comparison between images.

Statistical analysis

Data are expressed as mean ± standard error (SE) calculated over a minimum of three separate experiments. Statistical significance was determined using Student’s t test.

Results

Bacterial growth with 5HT, SP and Epi

The growth of P. fluorescens MFN1032 with 10−6 or 10−3 M of 5HT (Fig. 1a), SP (Fig. 1b) or Epi (Fig. 1c) was monitored for 24 h. The results show that the three molecules tested had only few effects on the growth of P. fluorescens MFN1032. Lag phase and growth rate were not affected. This result indicates that if virulence is enhanced in the next experiments of our study, it could not be directly attributed to bacterial overgrowth.
Fig. 1

Effect of 5HT, SP and Epi (10−6 and 10−3 M) on the growth of P. fluorescens MFN1032

Swimming and swarming motility tests

Swimming and swarming motilities were studied using 0.3 and 0.6 % agar in petri dishes. The migration distances of P. fluorescens MFN1032 pretreated or not with 5HT, SP or Epi were measured after 24 h incubation (Fig. 2). It appeared that only 5HT modulated significantly the swimming motility of P. fluorescens MFN1032. Indeed, untreated bacteria swam 5.7 ± 0.3 cm, whereas they reached 7.2 ± 0.3 cm after 5HT treatment. Conversely, the three molecules tested increased the swarming motility of P. fluorescens MFN1032, reaching 5.8 ± 0.3, 6.3 ± 0.4 and 6.5 ± 0.2 cm, in the presence of 5HT, SP and Epi, respectively, compared to 4.6 ± 0.1 cm for the untreated bacteria.
Fig. 2

Effect of 5HT, SP and Epi (10−6 M) on swimming (a) and swarming (b) motilities of P. fluorescens MFN1032. Y axis indicates the distance traveled (cm) by the bacteria. NS not significant, **P < 0.01, ***P < 0.001, versus untreated bacteria

Production of pyoverdin

Pyoverdin is a siderophore and virulence factor essential for the colonization of bacteria belonging to Pseudomonas genus (Meyer et al. 1996). Here, we investigated the effect of 5HT, SP and Epi on the production of pyoverdin by P. fluorescens MFN1032 after 48 h of bacterial culture (Fig. 3). The results show that 5HT induced a decrease in pyoverdin production, whereas SP and Epi had no significant effect.
Fig. 3

Effect of 5HT, SP and Epi (10−6 M) on pyoverdin production by P. fluorescens MFN1032. Pyoverdin production is expressed as the ratio of pyoverdin adsorption (OD400nm) to the bacterial density (OD600nm). NS not significant, *P < 0.05, versus untreated bacteria

Cytotoxicity assay and IL-8 secretion

The cytotoxicity and pro-inflammatory potential of P. fluorescens MFN1032 treated with 5HT, SP or Epi were compared to untreated bacteria. We found that the cytotoxicity of P. fluorescens MFN1032 was not modified by any of the molecules tested (Fig. 4a), but when the bacteria were treated with SP before the infection of Caco-2/TC7 cells, the production of IL-8 was significantly increased (Fig. 4b).
Fig. 4

Effect of 5HT, SP and Epi (10−6 M) on P. fluorescens MFN1032 cytotoxic activity toward Caco-2/TC7 cells (a) and pro-inflammatory potential: activation of interleukin-8 (IL-8) secretion by Caco-2/TC7 cells (b). Cytotoxicity was evaluated by measurement of lactate dehydrogenase (LDH) released from damaged cells. NS not significant, **P < 0.01, versus cells infected by untreated bacteria

Transepithelial electrical resistance measurements

The effect of P. fluorescens MFN1032 on differentiated Caco-2/TC7 cells was evaluated after 18 h of infection (Fig. 5). The results show that the TER of the Caco-2/TC7 monolayers decreased more when the infection was done with the bacteria pretreated with SP or Epi than infection with the untreated bacteria. On the contrary, pretreatment of P. fluorescens MFN1032 with 5HT had no effect. This suggests that SP and Epi may enhance the damages of the monolayer provoked by the bacteria.
Fig. 5

Effect of P. fluorescens MFN1032 treated or not by 5HT, SP and Epi (10−6 M) on the transepithelial resistance (TER) of differentiated Caco-2/TC7 cell monolayers after 18 h of infection. The data are expressed as percentage of the initial TER, measured across the monolayer at the onset of the experiment. NS not significant, *P < 0.05, **P < 0.01, versus Caco-2/TC7 cell monolayers infected with untreated bacteria

Actin staining

To visualize the results obtained by TER measurements, F-actin cytoskeleton was stained and observed by confocal microscopy. Differentiated Caco-2/TC7 cells showed a well-defined network of F-actin (Fig. 6a). When the monolayer was infected with P. fluorescens MFN1032, the F-actin appeared partly disorganized (Fig. 6b), and the same result was obtained when P. fluorescens MFN1032 was exposed to 5HT before infection of Caco-2/TC7 cells (Fig. 6c). Conversely, a pretreatment of the bacteria by SP (Fig. 6d) or Epi (Fig. 6e) led to the disruption of cell-to-cell contact of the epithelium and the redistribution of some F-actin filaments to the cytoplasm. These damages of the Caco-2/TC7 monolayer are in agreement with the TER measurements.
Fig. 6

Effect of P. fluorescens MFN1032 treated or not by 5HT, SP and Epi (10−6 M) on the F-actin cytoskeleton of Caco-2/TC7 cells. F-actin cytoskeleton was stained with Alexa Fluor® 488 phalloidin and examined using a confocal laser scanning microscope. Uninfected Caco-2/TC7 cells (a), Caco-2/TC7 cells infected with P. fluorescens MFN1032 (b), Caco-2/TC7 cells infected with P. fluorescens MFN1032 treated by 5HT (c), Caco-2/TC7 cells infected with P. fluorescens MFN1032 treated by SP (d), Caco-2/TC7 cells infected with P. fluorescens MFN1032 treated by Epi (e)

Discussion

Although most widely studied for its role in the soil and the rhizosphere, P. fluorescens possesses a number of functional traits that provide it with the capability to grow and thrive in mammalian hosts. Multiple culture-based and culture-independent studies have identified it at low levels in the indigenous microbiota of various body sites. Although this germ is not generally considered as a bacterial pathogen in human, it has been associated with bacteremia and 54 % of Crohn’s disease patients were found to develop serum antibodies to P. fluorescens (Sutton et al. 2000). This suggests that association between humans and P. fluorescens during health and disease may be complex. This bacterium was recently found to be able to induce and divert the human β-defensin-2 secretion in intestinal epithelial cells to enhance its virulence (Madi et al. 2013). However, the effect of other intestinal molecules produced by the host on the virulence of P. fluorescens remains unknown. Our study shows for the first time that 5HT, SP and Epi can modulate the virulence behavior of the clinical strain P. fluorescens MFN1032, whereas its growth was feebly affected by these molecules even at high concentration level. Nevertheless, several eukaryotic molecules are known to be able to modulate positively or negatively the bacterial growth. High concentrations of SP (>10−4 M) have previously been shown to display both direct and indirect antimicrobial activities on several bacteria including E. coli and P. aeruginosa, by acting as a weak cationic antimicrobial peptide (Kowalska et al. 2002; Hansen et al. 2006; Lesouhaitier et al. 2009). Conversely, 5HT added to an E. coli K12 culture stimulates cell proliferation and biomass accumulation (Anuchin et al. 2008), and the authors of this study showed a nonlinear concentration dependence curve probably due to a specific receptor-/sensor-dependent mechanism. 5HT was also found to enhance the growth and cellular aggregation of other bacterial species including Streptococcus faecalis or eukaryotic microorganisms, such as the yeast Candida guillermondii (Strakhovskaia et al. 1993). Catecholamines, which include norepinephrine (NE), Epi and dopamine, are able to increase significantly the growth of P. aeruginosa, K. pneumoniae and E. coli (Belay and Sonnenfeld 2002), and this varies greatly among bacterial species (Belay et al. 2003). In our study, we found that even at concentrations much above those physiologically present in the host (10−3 M), the growth of P. fluorescens MFN1032 was not significantly affected by 5HT, SP and Epi, as previously observed for P. fluorescens with antimicrobial peptides (Madi et al. 2013), but also with γ-aminobutyric acid (GABA) (Dagorn et al. 2013) and natriuretic peptides (Veron et al. 2008).

We found that the modulation of virulence varied with the intestinal factor tested. SP and Epi were shown to increase the swarming motility of P. fluorescens MFN1032, while 5HT enhanced both the swimming and swarming capacities of the bacteria but led to a decrease in pyoverdin production. In E. coli O157:H7 (EHEC), Epi and NE were found to increase motility and biofilm formation (Bansal et al. 2007). In fact, the AI-3 quorum-sensing system is involved in interkingdom signaling with the eukaryotic hormones Epi/NE. This AI-3/Epi/NE signaling system activates transcription of virulence genes in EHEC (Clarke et al. 2006) and is also found in other gram-negative bacteria like Salmonella enterica serovar Typhimurium for which this system is a key factor of in vitro and in vivo pathogenesis (Moreira et al. 2010). In P. aeruginosa, NE may replace siderophore by providing iron and this could repress the production of siderophores like pyoverdin (Visca et al. 2002; Stintzi et al. 1999; Li et al. 2009).

None of the intestinal molecules tested significantly modulates the cytotoxicity of P. fluorescens MFN1032, but when the bacteria were pretreated with SP before infection of the Caco-2/TC7 cells, an increase in IL-8 secretion could be observed. Conversely, elevated necrotic activity has been found for P. fluorescens following treatment with natriuretic peptides (BNP, CNP) and GABA, and this was partially attributed to modifications in the LPS structure of the bacteria and surface properties (Veron et al. 2008; Dagorn et al. 2013). In addition, unlike our results, the cytotoxicity of Bacillus cereus has been found to be strongly stimulated after exposure to SP and increases in virulence in Staphylococcus aureus and Staphylococcus epidermidis were also observed (Mijouin et al. 2013).

A pretreatment of P. fluorescens MFN1032 with SP or Epi before infection of Caco-2/TC7 cells enhanced the permeability of the monolayer as shown by TER measurement and observation of the cells and F-actin by confocal microcopy. Indeed, Caco-2/TC7 monolayers were more damaged when infected with P. fluorescens MFN1032 pretreated by SP or Epi than after infection with the untreated bacteria. The same kind of effect was reported for Caco-2 cells infected with Campylobacter jejuni after treatment by NE (Cogan et al. 2007). Indeed, these authors found that when C. jejuni was grown in iron-limited media in the presence of NE, growth rate, motility and invasion of cultured epithelial cells were increased compared with cultures grown in the absence of the molecule. Bacteria exposed to NE during growth also caused greater subsequent disruption of cultured epithelial cell monolayers, inducing widespread breakdown of tight junctions.

In summary, our results demonstrate that the virulence behavior of P. fluorescens MFN1032 can be modulated by intestinal factors and this effect is molecule dependent. This suggests that intestinal molecules may be sensed by the gut microbiota and probably participate in health and disease. In the future, further studies should be necessary to investigate the mode of action of the enteroendocrine factors on P. fluorescens MFN1032 virulence and the modulation of the gut microbiota.

Notes

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

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Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Kelly Biaggini
    • 1
    • 2
  • Corinne Barbey
    • 1
  • Valérie Borrel
    • 1
  • Marc Feuilloley
    • 1
  • Pierre Déchelotte
    • 2
  • Nathalie Connil
    • 1
  1. 1.Laboratoire de Microbiologie, Signaux et Microenvironnement (LMSM) EA4312Université de RouenÉvreuxFrance
  2. 2.INSERM Unité 1073 «Nutrition, Inflammation et dysfonction de l’axe intestin-cerveau»Université de RouenRouenFrance

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