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Title: Stenotrophomonas maltophilia differential gene expression in synthetic cystic fibrosis sputum reveals shared and cystic fibrosis strain-specific responses to the sputum environment.

Abstract

Stenotrophomonas maltophilia is a Gram-negative opportunistic pathogen that can infect the lungs of people with cystic fibrosis (CF). The highly viscous mucus in the CF lung, expectorated as sputum, serves as the primary nutrient source for microbes colonizing this site and induces virulence-associated phenotypes and gene expression in several CF pathogens. Here, we characterized the transcriptional responses of three S. maltophilia strains during exposure to synthetic CF sputum media (SCFM2) to gain insight into how this organism interacts with the host in the CF lung. These efforts led to the identification of 881 transcripts differentially expressed by all three strains, many of which reflect the metabolic pathways used by S. maltophilia in sputum, as well as altered stress responses. The latter correlated with increased resistance to peroxide exposure after pre-growth in SCFM2 for two of the strains. We also compared the SCFM2 transcriptomes of two S. maltophilia CF isolates to that of the acute infection strain, S. maltophilia K279a, allowing us to identify CF isolate-specific signatures in differential gene expression. Expression of genes from the accessory genomes was also differentially altered in response to SCFM2. Finally, a number of biofilm-associated genes were differentially induced in SCFM2, particularly in K279a, whichmore » corresponded to increased aggregation and biofilm formation in this strain relative to both CF strains. Collectively, this work details the response ofS. maltophiliato an environment that mimics important aspects of the CF lung, identifying potential survival strategies and metabolic pathways used byS. maltophiliaduring infections.Importance Stenotrophomonas maltophilia is an important infecting bacterium in the airways of people with cystic fibrosis (CF). However, compared to the other CF pathogens, S. maltophilia has been relatively understudied. The significance of our research is to provide insight into the global transcriptomic changes of S. maltophilia in response to a medium that was designed to mimic important aspects of the CF lung. This work allows us to understand the overall metabolic changes that occur when S. maltophilia encounters the CF lung, and generates a roadmap of candidate genes to test using in vitro and in vivo models of CF.« less

Authors:
 [1];  [1];  [2];  [1];  [1];  [2];  [3]; ORCiD logo [1]
+ Show Author Affiliations
  1. Univ. of Vermont, Burlington, VT (United States)
  2. Sandia National Lab. (SNL-CA), Livermore, CA (United States)
  3. Univ. of Michigan Medical School, Ann Arbor, MI (United States)
Publication Date:
Research Org.:
Sandia National Lab. (SNL-CA), Livermore, CA (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1530532
Report Number(s):
SAND-2019-7061J
Journal ID: ISSN 0021-9193; 676680
Grant/Contract Number:  
AC04-94AL85000
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Bacteriology
Additional Journal Information:
Journal Volume: 201; Journal Issue: 15; Journal ID: ISSN 0021-9193
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Willsey, Graham G., Eckstrom, Korin, LaBauve, Annette E., Hinkel, Lauren A., Schutz, Kristin, Meagher, Robert J., LiPuma, John J., and Wargo, Matthew J. Stenotrophomonas maltophilia differential gene expression in synthetic cystic fibrosis sputum reveals shared and cystic fibrosis strain-specific responses to the sputum environment.. United States: N. p., 2019. Web. doi:10.1128/JB.00074-19.
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Willsey, Graham G., Eckstrom, Korin, LaBauve, Annette E., Hinkel, Lauren A., Schutz, Kristin, Meagher, Robert J., LiPuma, John J., & Wargo, Matthew J. Stenotrophomonas maltophilia differential gene expression in synthetic cystic fibrosis sputum reveals shared and cystic fibrosis strain-specific responses to the sputum environment.. United States. https://doi.org/10.1128/JB.00074-19
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Willsey, Graham G., Eckstrom, Korin, LaBauve, Annette E., Hinkel, Lauren A., Schutz, Kristin, Meagher, Robert J., LiPuma, John J., and Wargo, Matthew J. Mon . "Stenotrophomonas maltophilia differential gene expression in synthetic cystic fibrosis sputum reveals shared and cystic fibrosis strain-specific responses to the sputum environment.". United States. https://doi.org/10.1128/JB.00074-19. https://www.osti.gov/servlets/purl/1530532.
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@article{osti_1530532,
title = {Stenotrophomonas maltophilia differential gene expression in synthetic cystic fibrosis sputum reveals shared and cystic fibrosis strain-specific responses to the sputum environment.},
author = {Willsey, Graham G. and Eckstrom, Korin and LaBauve, Annette E. and Hinkel, Lauren A. and Schutz, Kristin and Meagher, Robert J. and LiPuma, John J. and Wargo, Matthew J.},
abstractNote = {Stenotrophomonas maltophilia is a Gram-negative opportunistic pathogen that can infect the lungs of people with cystic fibrosis (CF). The highly viscous mucus in the CF lung, expectorated as sputum, serves as the primary nutrient source for microbes colonizing this site and induces virulence-associated phenotypes and gene expression in several CF pathogens. Here, we characterized the transcriptional responses of three S. maltophilia strains during exposure to synthetic CF sputum media (SCFM2) to gain insight into how this organism interacts with the host in the CF lung. These efforts led to the identification of 881 transcripts differentially expressed by all three strains, many of which reflect the metabolic pathways used by S. maltophilia in sputum, as well as altered stress responses. The latter correlated with increased resistance to peroxide exposure after pre-growth in SCFM2 for two of the strains. We also compared the SCFM2 transcriptomes of two S. maltophilia CF isolates to that of the acute infection strain, S. maltophilia K279a, allowing us to identify CF isolate-specific signatures in differential gene expression. Expression of genes from the accessory genomes was also differentially altered in response to SCFM2. Finally, a number of biofilm-associated genes were differentially induced in SCFM2, particularly in K279a, which corresponded to increased aggregation and biofilm formation in this strain relative to both CF strains. Collectively, this work details the response ofS. maltophiliato an environment that mimics important aspects of the CF lung, identifying potential survival strategies and metabolic pathways used byS. maltophiliaduring infections.Importance Stenotrophomonas maltophilia is an important infecting bacterium in the airways of people with cystic fibrosis (CF). However, compared to the other CF pathogens, S. maltophilia has been relatively understudied. The significance of our research is to provide insight into the global transcriptomic changes of S. maltophilia in response to a medium that was designed to mimic important aspects of the CF lung. This work allows us to understand the overall metabolic changes that occur when S. maltophilia encounters the CF lung, and generates a roadmap of candidate genes to test using in vitro and in vivo models of CF.},
doi = {10.1128/JB.00074-19},
journal = {Journal of Bacteriology},
number = 15,
volume = 201,
place = {United States},
year = {Mon May 20 00:00:00 EDT 2019},
month = {Mon May 20 00:00:00 EDT 2019}
}
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https://doi.org/10.1128/JB.00074-19
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