Pyochelin biotransformation by Staphylococcus aureus shapes bacterial competition with Pseudomonas aeruginosa in polymicrobial infections
Summary: Pseudomonas aeruginosa and Staphylococcus aureus are among the most frequently isolated bacterial species from polymicrobial infections of patients with cystic fibrosis and chronic wounds. We apply mass spectrometry guided interaction studies to determine how chemical interaction shapes the...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2023-06-01
|
| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S221112472300551X |
| _version_ | 1797820692155072512 |
|---|---|
| author | Christian Jenul Klara C. Keim Justin N. Jens Michael J. Zeiler Katrin Schilcher Michael J. Schurr Christian Melander Vanessa V. Phelan Alexander R. Horswill |
| author_facet | Christian Jenul Klara C. Keim Justin N. Jens Michael J. Zeiler Katrin Schilcher Michael J. Schurr Christian Melander Vanessa V. Phelan Alexander R. Horswill |
| author_sort | Christian Jenul |
| collection | DOAJ |
| description | Summary: Pseudomonas aeruginosa and Staphylococcus aureus are among the most frequently isolated bacterial species from polymicrobial infections of patients with cystic fibrosis and chronic wounds. We apply mass spectrometry guided interaction studies to determine how chemical interaction shapes the fitness and community structure during co-infection of these two pathogens. We demonstrate that S. aureus is equipped with an elegant mechanism to inactivate pyochelin via the yet uncharacterized methyltransferase Spm (staphylococcal pyochelin methyltransferase). Methylation of pyochelin abolishes the siderophore activity of pyochelin and significantly lowers pyochelin-mediated intracellular reactive oxygen species (ROS) production in S. aureus. In a murine wound co-infection model, an S. aureus mutant unable to methylate pyochelin shows significantly lower fitness compared with its parental strain. Thus, Spm-mediated pyochelin methylation is a mechanism to increase S. aureus survival during in vivo competition with P. aeruginosa. |
| first_indexed | 2024-03-13T09:42:59Z |
| format | Article |
| id | doaj.art-edbf94cbfab746d385a8a5e167267dd4 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-03-13T09:42:59Z |
| publishDate | 2023-06-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-edbf94cbfab746d385a8a5e167267dd42023-05-25T04:24:15ZengElsevierCell Reports2211-12472023-06-01426112540Pyochelin biotransformation by Staphylococcus aureus shapes bacterial competition with Pseudomonas aeruginosa in polymicrobial infectionsChristian Jenul0Klara C. Keim1Justin N. Jens2Michael J. Zeiler3Katrin Schilcher4Michael J. Schurr5Christian Melander6Vanessa V. Phelan7Alexander R. Horswill8Department of Immunology and Microbiology, School of Medicine, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045, USA; Department of Genetics and Genome Biology, University of Leicester, Leicester LE1 7RH, UKDepartment of Immunology and Microbiology, School of Medicine, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045, USADepartment of Pharmaceutical Sciences, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045, USADepartment of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, IN 46556, USADepartment of Immunology and Microbiology, School of Medicine, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045, USA; Department of Genetics and Genome Biology, University of Leicester, Leicester LE1 7RH, UKDepartment of Immunology and Microbiology, School of Medicine, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045, USADepartment of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, IN 46556, USADepartment of Pharmaceutical Sciences, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045, USA; Corresponding authorDepartment of Immunology and Microbiology, School of Medicine, University of Colorado, Anschutz Medical Campus, Aurora, CO 80045, USA; Department of Veterans Affairs, Eastern Colorado Health Care System, Aurora, CO 80045, USA; Corresponding authorSummary: Pseudomonas aeruginosa and Staphylococcus aureus are among the most frequently isolated bacterial species from polymicrobial infections of patients with cystic fibrosis and chronic wounds. We apply mass spectrometry guided interaction studies to determine how chemical interaction shapes the fitness and community structure during co-infection of these two pathogens. We demonstrate that S. aureus is equipped with an elegant mechanism to inactivate pyochelin via the yet uncharacterized methyltransferase Spm (staphylococcal pyochelin methyltransferase). Methylation of pyochelin abolishes the siderophore activity of pyochelin and significantly lowers pyochelin-mediated intracellular reactive oxygen species (ROS) production in S. aureus. In a murine wound co-infection model, an S. aureus mutant unable to methylate pyochelin shows significantly lower fitness compared with its parental strain. Thus, Spm-mediated pyochelin methylation is a mechanism to increase S. aureus survival during in vivo competition with P. aeruginosa.http://www.sciencedirect.com/science/article/pii/S221112472300551XCP: Microbiology |
| spellingShingle | Christian Jenul Klara C. Keim Justin N. Jens Michael J. Zeiler Katrin Schilcher Michael J. Schurr Christian Melander Vanessa V. Phelan Alexander R. Horswill Pyochelin biotransformation by Staphylococcus aureus shapes bacterial competition with Pseudomonas aeruginosa in polymicrobial infections Cell Reports CP: Microbiology |
| title | Pyochelin biotransformation by Staphylococcus aureus shapes bacterial competition with Pseudomonas aeruginosa in polymicrobial infections |
| title_full | Pyochelin biotransformation by Staphylococcus aureus shapes bacterial competition with Pseudomonas aeruginosa in polymicrobial infections |
| title_fullStr | Pyochelin biotransformation by Staphylococcus aureus shapes bacterial competition with Pseudomonas aeruginosa in polymicrobial infections |
| title_full_unstemmed | Pyochelin biotransformation by Staphylococcus aureus shapes bacterial competition with Pseudomonas aeruginosa in polymicrobial infections |
| title_short | Pyochelin biotransformation by Staphylococcus aureus shapes bacterial competition with Pseudomonas aeruginosa in polymicrobial infections |
| title_sort | pyochelin biotransformation by staphylococcus aureus shapes bacterial competition with pseudomonas aeruginosa in polymicrobial infections |
| topic | CP: Microbiology |
| url | http://www.sciencedirect.com/science/article/pii/S221112472300551X |
| work_keys_str_mv | AT christianjenul pyochelinbiotransformationbystaphylococcusaureusshapesbacterialcompetitionwithpseudomonasaeruginosainpolymicrobialinfections AT klarackeim pyochelinbiotransformationbystaphylococcusaureusshapesbacterialcompetitionwithpseudomonasaeruginosainpolymicrobialinfections AT justinnjens pyochelinbiotransformationbystaphylococcusaureusshapesbacterialcompetitionwithpseudomonasaeruginosainpolymicrobialinfections AT michaeljzeiler pyochelinbiotransformationbystaphylococcusaureusshapesbacterialcompetitionwithpseudomonasaeruginosainpolymicrobialinfections AT katrinschilcher pyochelinbiotransformationbystaphylococcusaureusshapesbacterialcompetitionwithpseudomonasaeruginosainpolymicrobialinfections AT michaeljschurr pyochelinbiotransformationbystaphylococcusaureusshapesbacterialcompetitionwithpseudomonasaeruginosainpolymicrobialinfections AT christianmelander pyochelinbiotransformationbystaphylococcusaureusshapesbacterialcompetitionwithpseudomonasaeruginosainpolymicrobialinfections AT vanessavphelan pyochelinbiotransformationbystaphylococcusaureusshapesbacterialcompetitionwithpseudomonasaeruginosainpolymicrobialinfections AT alexanderrhorswill pyochelinbiotransformationbystaphylococcusaureusshapesbacterialcompetitionwithpseudomonasaeruginosainpolymicrobialinfections |