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Identification of the main glutamine and glutamate transporters in Staphylococcus aureus and their impact on c‐di‐AMP production

A Staphylococcus aureus strain deleted for the c‐di‐AMP cyclase gene dacA is unable to survive in rich medium unless it acquires compensatory mutations. Previously identified mutations were in opuD, encoding the main glycine‐betaine transporter, and alsT, encoding a predicted amino acid transporter....

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Autores principales: Zeden, Merve S., Kviatkovski, Igor, Schuster, Christopher F., Thomas, Vinai C., Fey, Paul D., Gründling, Angelika
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7299772/
https://www.ncbi.nlm.nih.gov/pubmed/31997474
http://dx.doi.org/10.1111/mmi.14479
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author Zeden, Merve S.
Kviatkovski, Igor
Schuster, Christopher F.
Thomas, Vinai C.
Fey, Paul D.
Gründling, Angelika
author_facet Zeden, Merve S.
Kviatkovski, Igor
Schuster, Christopher F.
Thomas, Vinai C.
Fey, Paul D.
Gründling, Angelika
author_sort Zeden, Merve S.
collection PubMed
description A Staphylococcus aureus strain deleted for the c‐di‐AMP cyclase gene dacA is unable to survive in rich medium unless it acquires compensatory mutations. Previously identified mutations were in opuD, encoding the main glycine‐betaine transporter, and alsT, encoding a predicted amino acid transporter. Here, we show that inactivation of OpuD restores the cell size of a dacA mutant to near wild‐type (WT) size, while inactivation of AlsT does not. AlsT was identified as an efficient glutamine transporter, indicating that preventing glutamine uptake in rich medium rescues the growth of the S. aureus dacA mutant. In addition, GltS was identified as a glutamate transporter. By performing growth curves with WT, alsT and gltS mutant strains in defined medium supplemented with ammonium, glutamine or glutamate, we revealed that ammonium and glutamine, but not glutamate promote the growth of S. aureus. This suggests that besides ammonium also glutamine can serve as a nitrogen source under these conditions. Ammonium and uptake of glutamine via AlsT and hence likely a higher intracellular glutamine concentration inhibited c‐di‐AMP production, while glutamate uptake had no effect. These findings provide, besides the previously reported link between potassium and osmolyte uptake, a connection between nitrogen metabolism and c‐di‐AMP signalling in S. aureus.
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spelling pubmed-72997722020-06-29 Identification of the main glutamine and glutamate transporters in Staphylococcus aureus and their impact on c‐di‐AMP production Zeden, Merve S. Kviatkovski, Igor Schuster, Christopher F. Thomas, Vinai C. Fey, Paul D. Gründling, Angelika Mol Microbiol Research Articles A Staphylococcus aureus strain deleted for the c‐di‐AMP cyclase gene dacA is unable to survive in rich medium unless it acquires compensatory mutations. Previously identified mutations were in opuD, encoding the main glycine‐betaine transporter, and alsT, encoding a predicted amino acid transporter. Here, we show that inactivation of OpuD restores the cell size of a dacA mutant to near wild‐type (WT) size, while inactivation of AlsT does not. AlsT was identified as an efficient glutamine transporter, indicating that preventing glutamine uptake in rich medium rescues the growth of the S. aureus dacA mutant. In addition, GltS was identified as a glutamate transporter. By performing growth curves with WT, alsT and gltS mutant strains in defined medium supplemented with ammonium, glutamine or glutamate, we revealed that ammonium and glutamine, but not glutamate promote the growth of S. aureus. This suggests that besides ammonium also glutamine can serve as a nitrogen source under these conditions. Ammonium and uptake of glutamine via AlsT and hence likely a higher intracellular glutamine concentration inhibited c‐di‐AMP production, while glutamate uptake had no effect. These findings provide, besides the previously reported link between potassium and osmolyte uptake, a connection between nitrogen metabolism and c‐di‐AMP signalling in S. aureus. John Wiley and Sons Inc. 2020-02-11 2020-06 /pmc/articles/PMC7299772/ /pubmed/31997474 http://dx.doi.org/10.1111/mmi.14479 Text en © 2020 The Authors. Molecular Microbiology published by John Wiley & Sons Ltd This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Zeden, Merve S.
Kviatkovski, Igor
Schuster, Christopher F.
Thomas, Vinai C.
Fey, Paul D.
Gründling, Angelika
Identification of the main glutamine and glutamate transporters in Staphylococcus aureus and their impact on c‐di‐AMP production
title Identification of the main glutamine and glutamate transporters in Staphylococcus aureus and their impact on c‐di‐AMP production
title_full Identification of the main glutamine and glutamate transporters in Staphylococcus aureus and their impact on c‐di‐AMP production
title_fullStr Identification of the main glutamine and glutamate transporters in Staphylococcus aureus and their impact on c‐di‐AMP production
title_full_unstemmed Identification of the main glutamine and glutamate transporters in Staphylococcus aureus and their impact on c‐di‐AMP production
title_short Identification of the main glutamine and glutamate transporters in Staphylococcus aureus and their impact on c‐di‐AMP production
title_sort identification of the main glutamine and glutamate transporters in staphylococcus aureus and their impact on c‐di‐amp production
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7299772/
https://www.ncbi.nlm.nih.gov/pubmed/31997474
http://dx.doi.org/10.1111/mmi.14479
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