Tracking Polymicrobial Metabolism in Cystic Fibrosis Airways: <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Metabolism and Physiology Are Influenced by <named-content content-type="genus-species">Rothia mucilaginosa</named-content>-Derived Metabolites
ABSTRACT Due to a lack of effective immune clearance, the airways of cystic fibrosis patients are colonized by polymicrobial communities. One of the most widespread and destructive opportunistic pathogens is Pseudomonas aeruginosa; however, P. aeruginosa does not colonize the airways alone. Microbes...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2018-04-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphere.00151-18 |
| _version_ | 1818931323304148992 |
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| author | Bei Gao Tara Gallagher Ying Zhang Mona Elbadawi-Sidhu Zijuan Lai Oliver Fiehn Katrine L. Whiteson |
| author_facet | Bei Gao Tara Gallagher Ying Zhang Mona Elbadawi-Sidhu Zijuan Lai Oliver Fiehn Katrine L. Whiteson |
| author_sort | Bei Gao |
| collection | DOAJ |
| description | ABSTRACT Due to a lack of effective immune clearance, the airways of cystic fibrosis patients are colonized by polymicrobial communities. One of the most widespread and destructive opportunistic pathogens is Pseudomonas aeruginosa; however, P. aeruginosa does not colonize the airways alone. Microbes that are common in the oral cavity, such as Rothia mucilaginosa, are also present in cystic fibrosis patient sputum and have metabolic capacities different from those of P. aeruginosa. Here we examine the metabolic interactions of P. aeruginosa and R. mucilaginosa using stable-isotope-assisted metabolomics. Glucose-derived 13C was incorporated into glycolysis metabolites, namely, lactate and acetate, and some amino acids in R. mucilaginosa grown aerobically and anaerobically. The amino acid glutamate was unlabeled in the R. mucilaginosa supernatant but incorporated the 13C label after P. aeruginosa was cross-fed the R. mucilaginosa supernatant in minimal medium and artificial-sputum medium. We provide evidence that P. aeruginosa utilizes R. mucilaginosa-produced metabolites as precursors for generation of primary metabolites, including glutamate. IMPORTANCE Pseudomonas aeruginosa is a dominant and persistent cystic fibrosis pathogen. Although P. aeruginosa is accompanied by other microbes in the airways of cystic fibrosis patients, few cystic fibrosis studies show how P. aeruginosa is affected by the metabolism of other bacteria. Here, we demonstrate that P. aeruginosa generates primary metabolites using substrates produced by another microbe that is prevalent in the airways of cystic fibrosis patients, Rothia mucilaginosa. These results indicate that P. aeruginosa may get a metabolic boost from its microbial neighbor, which might contribute to its pathogenesis in the airways of cystic fibrosis patients. |
| first_indexed | 2024-12-20T04:14:46Z |
| format | Article |
| id | doaj.art-9ad2cbd7d6ee4191b8bd25deaee90ba4 |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-20T04:14:46Z |
| publishDate | 2018-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-9ad2cbd7d6ee4191b8bd25deaee90ba42022-12-21T19:53:48ZengAmerican Society for MicrobiologymSphere2379-50422018-04-013210.1128/mSphere.00151-18Tracking Polymicrobial Metabolism in Cystic Fibrosis Airways: <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Metabolism and Physiology Are Influenced by <named-content content-type="genus-species">Rothia mucilaginosa</named-content>-Derived MetabolitesBei Gao0Tara Gallagher1Ying Zhang2Mona Elbadawi-Sidhu3Zijuan Lai4Oliver Fiehn5Katrine L. Whiteson6NIH West Coast Metabolomics Center, University of California, Davis, California, USADepartment of Molecular Biology and Biochemistry, University of California, Irvine, California, USANIH West Coast Metabolomics Center, University of California, Davis, California, USANIH West Coast Metabolomics Center, University of California, Davis, California, USANIH West Coast Metabolomics Center, University of California, Davis, California, USANIH West Coast Metabolomics Center, University of California, Davis, California, USADepartment of Molecular Biology and Biochemistry, University of California, Irvine, California, USAABSTRACT Due to a lack of effective immune clearance, the airways of cystic fibrosis patients are colonized by polymicrobial communities. One of the most widespread and destructive opportunistic pathogens is Pseudomonas aeruginosa; however, P. aeruginosa does not colonize the airways alone. Microbes that are common in the oral cavity, such as Rothia mucilaginosa, are also present in cystic fibrosis patient sputum and have metabolic capacities different from those of P. aeruginosa. Here we examine the metabolic interactions of P. aeruginosa and R. mucilaginosa using stable-isotope-assisted metabolomics. Glucose-derived 13C was incorporated into glycolysis metabolites, namely, lactate and acetate, and some amino acids in R. mucilaginosa grown aerobically and anaerobically. The amino acid glutamate was unlabeled in the R. mucilaginosa supernatant but incorporated the 13C label after P. aeruginosa was cross-fed the R. mucilaginosa supernatant in minimal medium and artificial-sputum medium. We provide evidence that P. aeruginosa utilizes R. mucilaginosa-produced metabolites as precursors for generation of primary metabolites, including glutamate. IMPORTANCE Pseudomonas aeruginosa is a dominant and persistent cystic fibrosis pathogen. Although P. aeruginosa is accompanied by other microbes in the airways of cystic fibrosis patients, few cystic fibrosis studies show how P. aeruginosa is affected by the metabolism of other bacteria. Here, we demonstrate that P. aeruginosa generates primary metabolites using substrates produced by another microbe that is prevalent in the airways of cystic fibrosis patients, Rothia mucilaginosa. These results indicate that P. aeruginosa may get a metabolic boost from its microbial neighbor, which might contribute to its pathogenesis in the airways of cystic fibrosis patients.https://journals.asm.org/doi/10.1128/mSphere.00151-18Pseudomonas aeruginosaRothia mucilaginosametabolite cross-feedingmicrobial interactionspolymicrobial infectionsstable-isotope-assisted metabolomics |
| spellingShingle | Bei Gao Tara Gallagher Ying Zhang Mona Elbadawi-Sidhu Zijuan Lai Oliver Fiehn Katrine L. Whiteson Tracking Polymicrobial Metabolism in Cystic Fibrosis Airways: <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Metabolism and Physiology Are Influenced by <named-content content-type="genus-species">Rothia mucilaginosa</named-content>-Derived Metabolites mSphere Pseudomonas aeruginosa Rothia mucilaginosa metabolite cross-feeding microbial interactions polymicrobial infections stable-isotope-assisted metabolomics |
| title | Tracking Polymicrobial Metabolism in Cystic Fibrosis Airways: <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Metabolism and Physiology Are Influenced by <named-content content-type="genus-species">Rothia mucilaginosa</named-content>-Derived Metabolites |
| title_full | Tracking Polymicrobial Metabolism in Cystic Fibrosis Airways: <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Metabolism and Physiology Are Influenced by <named-content content-type="genus-species">Rothia mucilaginosa</named-content>-Derived Metabolites |
| title_fullStr | Tracking Polymicrobial Metabolism in Cystic Fibrosis Airways: <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Metabolism and Physiology Are Influenced by <named-content content-type="genus-species">Rothia mucilaginosa</named-content>-Derived Metabolites |
| title_full_unstemmed | Tracking Polymicrobial Metabolism in Cystic Fibrosis Airways: <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Metabolism and Physiology Are Influenced by <named-content content-type="genus-species">Rothia mucilaginosa</named-content>-Derived Metabolites |
| title_short | Tracking Polymicrobial Metabolism in Cystic Fibrosis Airways: <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Metabolism and Physiology Are Influenced by <named-content content-type="genus-species">Rothia mucilaginosa</named-content>-Derived Metabolites |
| title_sort | tracking polymicrobial metabolism in cystic fibrosis airways named content content type genus species pseudomonas aeruginosa named content metabolism and physiology are influenced by named content content type genus species rothia mucilaginosa named content derived metabolites |
| topic | Pseudomonas aeruginosa Rothia mucilaginosa metabolite cross-feeding microbial interactions polymicrobial infections stable-isotope-assisted metabolomics |
| url | https://journals.asm.org/doi/10.1128/mSphere.00151-18 |
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