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Research Article

Stenotrophomonas maltophilia Differential Gene Expression in Synthetic Cystic Fibrosis Sputum Reveals Shared and Cystic Fibrosis Strain-Specific Responses to the Sputum Environment

Graham G. Willsey, Korin Eckstrom, Annette E. LaBauve, Lauren A. Hinkel, Kristin Schutz, Robert J. Meagher, John J. LiPuma, Matthew J. Wargo
Michael Y. Galperin, Editor
Graham G. Willsey
aDepartment of Microbiology and Molecular Genetics, University of Vermont Larner College of Medicine, Burlington, Vermont, USA
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Korin Eckstrom
aDepartment of Microbiology and Molecular Genetics, University of Vermont Larner College of Medicine, Burlington, Vermont, USA
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Annette E. LaBauve
bBiotechnology and Bioengineering Department, Sandia National Laboratories, Livermore, California, USA
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Lauren A. Hinkel
aDepartment of Microbiology and Molecular Genetics, University of Vermont Larner College of Medicine, Burlington, Vermont, USA
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Kristin Schutz
aDepartment of Microbiology and Molecular Genetics, University of Vermont Larner College of Medicine, Burlington, Vermont, USA
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Robert J. Meagher
bBiotechnology and Bioengineering Department, Sandia National Laboratories, Livermore, California, USA
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John J. LiPuma
cDepartment of Pediatrics, University of Michigan Medical School, Ann Arbor, Michigan, USA
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Matthew J. Wargo
aDepartment of Microbiology and Molecular Genetics, University of Vermont Larner College of Medicine, Burlington, Vermont, USA
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Michael Y. Galperin
NCBI, NLM, National Institutes of Health
Roles: Editor
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DOI: 10.1128/JB.00074-19
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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 medium (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 pregrowth 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. The 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 of S. maltophilia to an environment that mimics important aspects of the CF lung, identifying potential survival strategies and metabolic pathways used by S. maltophilia during 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 study elucidates the overall metabolic changes that occur when S. maltophilia encounters the CF lung and generates a road map of candidate genes to test using in vitro and in vivo models of CF.

FOOTNOTES

    • Received 24 January 2019.
    • Accepted 14 May 2019.
    • Accepted manuscript posted online 20 May 2019.
  • Supplemental material for this article may be found at https://doi.org/10.1128/JB.00074-19.

  • Copyright © 2019 American Society for Microbiology.

All Rights Reserved.

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Stenotrophomonas maltophilia Differential Gene Expression in Synthetic Cystic Fibrosis Sputum Reveals Shared and Cystic Fibrosis Strain-Specific Responses to the Sputum Environment
Graham G. Willsey, Korin Eckstrom, Annette E. LaBauve, Lauren A. Hinkel, Kristin Schutz, Robert J. Meagher, John J. LiPuma, Matthew J. Wargo
Journal of Bacteriology Jul 2019, 201 (15) e00074-19; DOI: 10.1128/JB.00074-19

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Stenotrophomonas maltophilia Differential Gene Expression in Synthetic Cystic Fibrosis Sputum Reveals Shared and Cystic Fibrosis Strain-Specific Responses to the Sputum Environment
Graham G. Willsey, Korin Eckstrom, Annette E. LaBauve, Lauren A. Hinkel, Kristin Schutz, Robert J. Meagher, John J. LiPuma, Matthew J. Wargo
Journal of Bacteriology Jul 2019, 201 (15) e00074-19; DOI: 10.1128/JB.00074-19
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KEYWORDS

Stenotrophomonas
cystic fibrosis
metabolism
nutrient acquisition
transcriptional regulation
virulence factors

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