Experimentally evolved Staphylococcus aureus shows increased survival in the presence of Pseudomonas aeruginosa by acquiring mutations in the amino acid transporter, GltT

Author:

Alexander Ashley M.123ORCID,Luu Justin M.43ORCID,Raghuram Vishnu431ORCID,Bottacin Giulia5ORCID,van Vliet Simon65ORCID,Read Timothy D.1ORCID,Goldberg Joanna B.3ORCID

Affiliation:

1. Division of Infectious Diseases and Department of Human Genetics, Emory University School of Medicine, Atlanta, Georgia, USA

2. Population Biology, Ecology, and Evolution Program, Graduate Division of Biological and Biomedical Sciences, Laney Graduate School, Emory University, Atlanta, Georgia, USA

3. Department of Pediatrics, Division of Pulmonary, Asthma, Cystic Fibrosis, and Sleep, Emory University School of Medicine, Atlanta, Georgia, USA

4. Microbiology and Molecular Genetics Program, Graduate Division of Biological and Biomedical Sciences, Laney Graduate School, Emory University, Atlanta, Georgia, USA

5. Biozentrum, University of Basel, Spitalstrasse 41,4056 Basel, Switzerland

6. Department of Fundamental Microbiology, University of Lausanne, Quartier Unil-Sorge, 1015 Lausanne, Switzerland

Abstract

When cultured together under standard laboratory conditions Pseudomonas aeruginosa has been shown to be an effective inhibitor of Staphylococcus aureus. However, P. aeruginosa and S. aureus are commonly observed in coinfections of individuals with cystic fibrosis (CF) and in chronic wounds. Previous work from our group revealed that S. aureus isolates from CF infections are able to persist in the presence of P. aeruginosa strain PAO1 with a range of tolerances with some isolates being eliminated entirely and others maintaining large populations. In this study, we designed a serial transfer, evolution experiment to identify mutations that allow S. aureus to survive in the presence of P. aeruginosa. Using S. aureus USA300 JE2 as our ancestral strain, populations of S. aureus were repeatedly cocultured with fresh P. aeruginosa PAO1. After eight coculture periods, S. aureus populations that survived better in the presence of PAO1 were observed. We found two independent mutations in the highly conserved S. aureus aspartate transporter, gltT, that were unique to evolved P. aeruginosa-tolerant isolates. Subsequent phenotypic testing demonstrated that gltT mutants have reduced uptake of glutamate and outcompeted wild-type S. aureus when glutamate was absent from chemically defined media. These findings together demonstrate that the presence of P. aeruginosa exerts selective pressure on S. aureus to alter its uptake and metabolism of key amino acids when the two are cultured together.

Funder

National Institutes of Health

Cystic Fibrosis Foundation

Swiss National Science Foundation

Publisher

Microbiology Society

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