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Cooperative pathogenicity in cystic fibrosis: Stenotrophomonas maltophilia modulates Pseudomonas aeruginosa virulence in mixed biofilm.

Pompilio A, Crocetta V, De Nicola S, Verginelli F, Fiscarelli E, Di Bonaventura G - Front Microbiol (2015)

Bottom Line: Conversely, no effect was observed on P. aeruginosa by S. maltophilia.Compared with monocultures, the adhesiveness of P. aeruginosa on CFBE41o- cells was significantly reduced by S. maltophilia, which probably acts by reducing P. aeruginosa's swimming motility.Taken together, our results suggest that the existence of reciprocal interference of S. maltophilia and P. aeruginosa in CF lung is plausible.

View Article: PubMed Central - PubMed

Affiliation: Department of Medical, Oral and Biotechnological Sciences, "G. d'Annunzio" University of Chieti-Pescara Chieti, Italy ; Aging Research Center (Ce.S.I.), "G. d'Annunzio" University Foundation Chieti, Italy.

ABSTRACT
The present study was undertaken in order to understand more about the interaction occurring between S. maltophilia and P. aeruginosa, which are frequently co-isolated from CF airways. For this purpose, S. maltophilia RR7 and P. aeruginosa RR8 strains, co-isolated from the lung of a chronically infected CF patient during a pulmonary exacerbation episode, were evaluated for reciprocal effect during planktonic growth, adhesion and biofilm formation onto both polystyrene and CF bronchial cell monolayer, motility, as well as for gene expression in mixed biofilms. P. aeruginosa significantly affected S. maltophilia growth in both planktonic and biofilm cultures, due to an inhibitory activity probably requiring direct contact. Conversely, no effect was observed on P. aeruginosa by S. maltophilia. Compared with monocultures, the adhesiveness of P. aeruginosa on CFBE41o- cells was significantly reduced by S. maltophilia, which probably acts by reducing P. aeruginosa's swimming motility. An opposite trend was observed for biofilm formation, confirming the findings obtained using polystyrene. When grown in mixed biofilm with S. maltophilia, P. aeruginosa significantly over-expressed aprA, and algD-codifying for protease and alginate, respectively-while the quorum sensing related rhlR and lasI genes were down-regulated. The induced alginate expression by P. aeruginosa might be responsible for the protection of S. maltophilia against tobramycin activity we observed in mixed biofilms. Taken together, our results suggest that the existence of reciprocal interference of S. maltophilia and P. aeruginosa in CF lung is plausible. In particular, S. maltophilia might confer some selective "fitness advantage" to P. aeruginosa under the specific conditions of chronic infection or, alternatively, increase the virulence of P. aeruginosa thus leading to pulmonary exacerbation.

No MeSH data available.


Related in: MedlinePlus

Kinetics of planktonic growth exhibited by S. maltophilia RR7 and P. aeruginosa RR8, considered both as alone and in combination. S. maltophilia RR7 and P. aeruginosa RR8 were grown for 24 h in CAMHB in single culture and in co-culture after inoculation at equal ratio from mid-exponential phase pure cultures. Growth rate was monitored by colony count after plating on selective media for both species. (A) Growth curves of S. maltophilia RR7 and P. aeruginosa RR8 strains in pure culture (RR7, RR8) and in co-culture (RR7combi, RR8combi). The results are shown as mean + SD (n = 6). *p < 0.05, **p < 0.01, RR7 vs. RR8; §p < 0.05, RR8 vs. RR8combi; ∧p < 0.05, ∧∧p < 0.01, RR7 vs. RR7combi; ANOVA + Newman-Keuls post-test. (B) Competitive index (CI; black bars) and Relative Increase Ratio (RIR; gray bars) calculated from single and dual planktonic cultures of S. maltophilia RR7 and P. aeruginosa RR8 strains. The results are shown as mean ± SD (n = 6). *p < 0.05, **p < 0.01, CI vs. RIR, unpaired t-test. (C) Evaluation of antibacterial activity using agar spot assay. S. maltophilia RR7 vs. P. aeruginosa RR8 (left): no antibacterial activity. P. aeruginosa RR8 vs. S. maltophilia RR7 (right): partial antibacterial activity, as suggested by the regrowth observed within the inhibition zone. (D) Transwell assay: S. maltophilia RR7 growth without or with (exp) P. aeruginosa RR8. The results are expressed as mean + SD (n = 6).
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Figure 1: Kinetics of planktonic growth exhibited by S. maltophilia RR7 and P. aeruginosa RR8, considered both as alone and in combination. S. maltophilia RR7 and P. aeruginosa RR8 were grown for 24 h in CAMHB in single culture and in co-culture after inoculation at equal ratio from mid-exponential phase pure cultures. Growth rate was monitored by colony count after plating on selective media for both species. (A) Growth curves of S. maltophilia RR7 and P. aeruginosa RR8 strains in pure culture (RR7, RR8) and in co-culture (RR7combi, RR8combi). The results are shown as mean + SD (n = 6). *p < 0.05, **p < 0.01, RR7 vs. RR8; §p < 0.05, RR8 vs. RR8combi; ∧p < 0.05, ∧∧p < 0.01, RR7 vs. RR7combi; ANOVA + Newman-Keuls post-test. (B) Competitive index (CI; black bars) and Relative Increase Ratio (RIR; gray bars) calculated from single and dual planktonic cultures of S. maltophilia RR7 and P. aeruginosa RR8 strains. The results are shown as mean ± SD (n = 6). *p < 0.05, **p < 0.01, CI vs. RIR, unpaired t-test. (C) Evaluation of antibacterial activity using agar spot assay. S. maltophilia RR7 vs. P. aeruginosa RR8 (left): no antibacterial activity. P. aeruginosa RR8 vs. S. maltophilia RR7 (right): partial antibacterial activity, as suggested by the regrowth observed within the inhibition zone. (D) Transwell assay: S. maltophilia RR7 growth without or with (exp) P. aeruginosa RR8. The results are expressed as mean + SD (n = 6).

Mentions: The growth curve kinetics of P. aeruginosa RR8 and S. maltophilia RR7 strains, tested as alone or in mixed culture, were assessed by colony count over 24 h, and the results are shown in Figure 1A. When grown in mixed cultures, the growth kinetics of the two strains were comparable. However, compared with single cultures, the growth of both S. maltophilia RR7 and P. aeruginosa RR8 in mixed cultures was negatively affected during both log and stationary phases.


Cooperative pathogenicity in cystic fibrosis: Stenotrophomonas maltophilia modulates Pseudomonas aeruginosa virulence in mixed biofilm.

Pompilio A, Crocetta V, De Nicola S, Verginelli F, Fiscarelli E, Di Bonaventura G - Front Microbiol (2015)

Kinetics of planktonic growth exhibited by S. maltophilia RR7 and P. aeruginosa RR8, considered both as alone and in combination. S. maltophilia RR7 and P. aeruginosa RR8 were grown for 24 h in CAMHB in single culture and in co-culture after inoculation at equal ratio from mid-exponential phase pure cultures. Growth rate was monitored by colony count after plating on selective media for both species. (A) Growth curves of S. maltophilia RR7 and P. aeruginosa RR8 strains in pure culture (RR7, RR8) and in co-culture (RR7combi, RR8combi). The results are shown as mean + SD (n = 6). *p < 0.05, **p < 0.01, RR7 vs. RR8; §p < 0.05, RR8 vs. RR8combi; ∧p < 0.05, ∧∧p < 0.01, RR7 vs. RR7combi; ANOVA + Newman-Keuls post-test. (B) Competitive index (CI; black bars) and Relative Increase Ratio (RIR; gray bars) calculated from single and dual planktonic cultures of S. maltophilia RR7 and P. aeruginosa RR8 strains. The results are shown as mean ± SD (n = 6). *p < 0.05, **p < 0.01, CI vs. RIR, unpaired t-test. (C) Evaluation of antibacterial activity using agar spot assay. S. maltophilia RR7 vs. P. aeruginosa RR8 (left): no antibacterial activity. P. aeruginosa RR8 vs. S. maltophilia RR7 (right): partial antibacterial activity, as suggested by the regrowth observed within the inhibition zone. (D) Transwell assay: S. maltophilia RR7 growth without or with (exp) P. aeruginosa RR8. The results are expressed as mean + SD (n = 6).
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Related In: Results  -  Collection

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Figure 1: Kinetics of planktonic growth exhibited by S. maltophilia RR7 and P. aeruginosa RR8, considered both as alone and in combination. S. maltophilia RR7 and P. aeruginosa RR8 were grown for 24 h in CAMHB in single culture and in co-culture after inoculation at equal ratio from mid-exponential phase pure cultures. Growth rate was monitored by colony count after plating on selective media for both species. (A) Growth curves of S. maltophilia RR7 and P. aeruginosa RR8 strains in pure culture (RR7, RR8) and in co-culture (RR7combi, RR8combi). The results are shown as mean + SD (n = 6). *p < 0.05, **p < 0.01, RR7 vs. RR8; §p < 0.05, RR8 vs. RR8combi; ∧p < 0.05, ∧∧p < 0.01, RR7 vs. RR7combi; ANOVA + Newman-Keuls post-test. (B) Competitive index (CI; black bars) and Relative Increase Ratio (RIR; gray bars) calculated from single and dual planktonic cultures of S. maltophilia RR7 and P. aeruginosa RR8 strains. The results are shown as mean ± SD (n = 6). *p < 0.05, **p < 0.01, CI vs. RIR, unpaired t-test. (C) Evaluation of antibacterial activity using agar spot assay. S. maltophilia RR7 vs. P. aeruginosa RR8 (left): no antibacterial activity. P. aeruginosa RR8 vs. S. maltophilia RR7 (right): partial antibacterial activity, as suggested by the regrowth observed within the inhibition zone. (D) Transwell assay: S. maltophilia RR7 growth without or with (exp) P. aeruginosa RR8. The results are expressed as mean + SD (n = 6).
Mentions: The growth curve kinetics of P. aeruginosa RR8 and S. maltophilia RR7 strains, tested as alone or in mixed culture, were assessed by colony count over 24 h, and the results are shown in Figure 1A. When grown in mixed cultures, the growth kinetics of the two strains were comparable. However, compared with single cultures, the growth of both S. maltophilia RR7 and P. aeruginosa RR8 in mixed cultures was negatively affected during both log and stationary phases.

Bottom Line: Conversely, no effect was observed on P. aeruginosa by S. maltophilia.Compared with monocultures, the adhesiveness of P. aeruginosa on CFBE41o- cells was significantly reduced by S. maltophilia, which probably acts by reducing P. aeruginosa's swimming motility.Taken together, our results suggest that the existence of reciprocal interference of S. maltophilia and P. aeruginosa in CF lung is plausible.

View Article: PubMed Central - PubMed

Affiliation: Department of Medical, Oral and Biotechnological Sciences, "G. d'Annunzio" University of Chieti-Pescara Chieti, Italy ; Aging Research Center (Ce.S.I.), "G. d'Annunzio" University Foundation Chieti, Italy.

ABSTRACT
The present study was undertaken in order to understand more about the interaction occurring between S. maltophilia and P. aeruginosa, which are frequently co-isolated from CF airways. For this purpose, S. maltophilia RR7 and P. aeruginosa RR8 strains, co-isolated from the lung of a chronically infected CF patient during a pulmonary exacerbation episode, were evaluated for reciprocal effect during planktonic growth, adhesion and biofilm formation onto both polystyrene and CF bronchial cell monolayer, motility, as well as for gene expression in mixed biofilms. P. aeruginosa significantly affected S. maltophilia growth in both planktonic and biofilm cultures, due to an inhibitory activity probably requiring direct contact. Conversely, no effect was observed on P. aeruginosa by S. maltophilia. Compared with monocultures, the adhesiveness of P. aeruginosa on CFBE41o- cells was significantly reduced by S. maltophilia, which probably acts by reducing P. aeruginosa's swimming motility. An opposite trend was observed for biofilm formation, confirming the findings obtained using polystyrene. When grown in mixed biofilm with S. maltophilia, P. aeruginosa significantly over-expressed aprA, and algD-codifying for protease and alginate, respectively-while the quorum sensing related rhlR and lasI genes were down-regulated. The induced alginate expression by P. aeruginosa might be responsible for the protection of S. maltophilia against tobramycin activity we observed in mixed biofilms. Taken together, our results suggest that the existence of reciprocal interference of S. maltophilia and P. aeruginosa in CF lung is plausible. In particular, S. maltophilia might confer some selective "fitness advantage" to P. aeruginosa under the specific conditions of chronic infection or, alternatively, increase the virulence of P. aeruginosa thus leading to pulmonary exacerbation.

No MeSH data available.


Related in: MedlinePlus