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

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.

Insights into Cystic Fibrosis Polymicrobial Consortia: The Role of Species Interactions in Biofilm Development, Phenotype, and Response to In-Use Antibiotics

“…The results from CI versus RIR suggested that I. limosus and S. maltophilia are, in a general point of view, outcompeted. These findings are in agreement with Pompilio et al (2015) that found that P. aeruginosa , in dual biofilms, significantly affect S. maltophilia growth. They also shown that, when grown with S. maltophilia in dual biofilms, some P. aeruginosa virulence factors, as alkaline protease and alginate, were up-regulated.…”

“…Data suggest a potential protective effect of P. aeruginosa over the other species against ciprofloxacin. Similar hints were pointed out by Pompilio et al (2015) as they stated that P. aeruginosa might be responsible for the protection of S. maltophilia against tobramycin in dual biofilms due to alginate overproducing. Moreover, data also shown that, independently of the reduced biomass noticed in P. aeruginosa + S. aureus and P. aeruginosa + I. limosus dual biofilms, the high number of biofilm-encased cells was enough to imply an increased tolerance on those consortia.…”

In Vitro Activity of Colistin and Trimethoprim/Sulfamethoxazole Against Consortia of Multidrug Resistant Non-Fermenting Gram-Negative Bacilli Isolated from Lower Respiratory Tract

“…Dominantly in cystic fibrosis several studies focused on interaction of P. aeruginosa with other bacterial species, but only a few have been published on the interaction between P. aeruginosa and S. maltophilia. It was found that S. maltophilia increases the risk of resistance of P. aeruginosa to polymyxin; beta-lactamase leaking from S. maltophilia enhances the growth of P. aeruginosa in the presence of beta-lactam antibiotic agents; S. maltophilia might confer a selective fitness advantage to P. aeruginosa and increase the virulence of P. aeruginosa (18). The interaction of A. baumannii and S. maltophilia is not discussed in the literature, except for their ability to increase each other's biofilm production (19).…”

Genotypic and Phenotypic Characterization of Stenotrophomonas maltophilia Strains from a Pediatric Tertiary Care Hospital in Serbia

“…Pseudomonas aeruginosa the major pathogen in the CF lung due to biofilm-growing mucoid (alginate-producing) strains, which confer resistance to the host defense mechanism. Pompilio et al [36] reported the prevalence of P . aeruginosa in mixed biofilm communities formed by P .…”