Abstract
The present study was carried out to understand the adaptive strategies developed by Stenotrophomonas maltophilia for chronic colonization of the cystic fibrosis (CF) lung. For this purpose, 13 temporally isolated strains from a single CF patient chronically infected over a 10-year period were systematically characterized for growth rate, biofilm formation, motility, mutation frequencies, antibiotic resistance, and pathogenicity. Pulsed-field gel electrophoresis (PFGE) showed over time the presence of two distinct groups, each consisting of two different pulsotypes. The pattern of evolution followed by S. maltophilia was dependent on pulsotype considered, with strains belonging to pulsotype 1.1 resulting to be the most adapted, being significantly changed in all traits considered. Generally, S. maltophilia adaptation to CF lung leads to increased growth rate and antibiotic resistance, whereas both in vivo and in vitro pathogenicity as well as biofilm formation were decreased. Overall, our results show for the first time that S. maltophilia can successfully adapt to a highly stressful environment such as CF lung by paying a “biological cost,” as suggested by the presence of relevant genotypic and phenotypic heterogeneity within bacterial population. S. maltophilia populations are, therefore, significantly complex and dynamic being able to fluctuate rapidly under changing selective pressures.
Highlights
Stenotrophomonas maltophilia is one of the most common emerging multi-drug resistant pathogens found in the lungs of people with cystic fibrosis (CF) where its prevalence is increasing (Amin and Waters, 2014; Green and Jones, 2015; Salsgiver et al, 2016)
It is unclear whether S. maltophilia colonizes the lungs of people with CF without adverse effect or Abbreviations: CF, cystic fibrosis; Trypticase Soy broth (TSB), Trypticase soy broth; MHA, Mueller-Hinton agar; Pulsed-field gel electrophoresis (PFGE), pulsed-field gel electrophoresis; MGT, mean generation time; Specific Biofilm Formation” (SBF), specific biofilm formation index; MOI, multiplicity of infection
We report for the first time that chronic S. maltophilia displays unusual adaptive plasticity by modulating its virulence and pathogenicity, yet exacerbating antibiotic resistance and other factors that augment its fitness in the CF lungs
Summary
Stenotrophomonas maltophilia is one of the most common emerging multi-drug resistant pathogens found in the lungs of people with cystic fibrosis (CF) where its prevalence is increasing (Amin and Waters, 2014; Green and Jones, 2015; Salsgiver et al, 2016). In a series of studies, we found evidence highly suggestive of the pathogenic role of S. maltophilia in CF patients This microorganism can grow as biofilm on abiotic surfaces (Di Bonaventura et al, 2004, 2007a,b; Pompilio et al, 2008) and on CF-derived epithelial monolayer (Pompilio et al, 2010), probably because of a selective adaptation to CF airways (Pompilio et al, 2011). In a murine model of acute respiratory infection we observed that S. maltophilia significantly contributes to the inflammatory process resulting in compromised respiratory function and death (Di Bonaventura et al, 2010)
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