Transcriptional Profiling of <named-content content-type="genus-species">Staphylococcus aureus</named-content> During Growth in 2 M NaCl Leads to Clarification of Physiological Roles for Kdp and Ktr K<sup>+</sup> Uptake Systems

ABSTRACT Staphylococcus aureus exhibits an unusually high level of osmotolerance and Na+ tolerance, properties that support survival in various host niches and in preserved foods. The genetic basis of these traits is not well understood. We compared the transcriptional profiles of S. aureus grown in...

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Autores principales:	Alexa Price-Whelan, Chun Kit Poon, Meredith A. Benson, Tess T. Eidem, Christelle M. Roux, Jeffrey M. Boyd, Paul M. Dunman, Victor J. Torres, Terry A. Krulwich
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Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/9b4328fbcb9c4b819ce98ffec2f6dcef
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spelling	oai:doaj.org-article:9b4328fbcb9c4b819ce98ffec2f6dcef2021-11-15T15:43:09ZTranscriptional Profiling of <named-content content-type="genus-species">Staphylococcus aureus</named-content> During Growth in 2 M NaCl Leads to Clarification of Physiological Roles for Kdp and Ktr K<sup>+</sup> Uptake Systems10.1128/mBio.00407-132150-7511https://doaj.org/article/9b4328fbcb9c4b819ce98ffec2f6dcef2013-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00407-13https://doaj.org/toc/2150-7511ABSTRACT Staphylococcus aureus exhibits an unusually high level of osmotolerance and Na+ tolerance, properties that support survival in various host niches and in preserved foods. The genetic basis of these traits is not well understood. We compared the transcriptional profiles of S. aureus grown in complex medium with and without 2 M NaCl. The stimulon for growth in high-osmolality media and Na+ included genes involved in uptake of K+, other compatible solutes, sialic acid, and sugars; capsule biosynthesis; and amino acid and central metabolism. Quantitative PCR analysis revealed that the loci responded differently from each other to high osmolality imposed by elevated NaCl versus sucrose. High-affinity K+ uptake (kdp) genes and capsule biosynthesis (cap5) genes required the two-component system KdpDE for full induction by osmotic stress, with kdpA induced more by NaCl and cap5B induced more by sucrose. Focusing on K+ importers, we identified three S. aureus genes belonging to the lower-affinity Trk/Ktr family that encode two membrane proteins (KtrB and KtrD) and one accessory protein (KtrC). In the absence of osmotic stress, the ktr gene transcripts were much more abundant than the kdpA transcript. Disruption of S. aureus kdpA caused a growth defect under low-K+ conditions, disruption of ktrC resulted in a significant defect in 2 M NaCl, and a ΔktrC ΔkdpA double mutant exhibited both phenotypes. Protective effects of S. aureus Ktr transporters at elevated NaCl are consistent with previous indications that both Na+ and osmolality challenges are mitigated by the maintenance of a high cytoplasmic K+ concentration. IMPORTANCE There is general agreement that the osmotolerance and Na+ tolerance of Staphylococcus aureus are unusually high for a nonhalophile and support its capacity for human colonization, pathogenesis, and growth in food. Nonetheless, the molecular basis for these properties is not well defined. The genome-wide response of S. aureus to a high concentration, 2 M, of NaCl revealed the upregulation of expected genes, such as those for transporters of compatible solutes that are widely implicated in supporting osmotolerance. A high-affinity potassium uptake system, KdpFABC, was upregulated, although it generally plays a physiological role under very low K+ conditions. At higher K+ concentrations, a lower-affinity and more highly expressed type of K+ transporter system, Ktr transporters, was shown to play a significant role in high Na+ tolerance. This study illustrates the importance of the K+ status of the cell for tolerance of Na+ by S. aureus and underscores the importance of monovalent cation cycles in this pathogen.Alexa Price-WhelanChun Kit PoonMeredith A. BensonTess T. EidemChristelle M. RouxJeffrey M. BoydPaul M. DunmanVictor J. TorresTerry A. KrulwichAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 4 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Alexa Price-Whelan Chun Kit Poon Meredith A. Benson Tess T. Eidem Christelle M. Roux Jeffrey M. Boyd Paul M. Dunman Victor J. Torres Terry A. Krulwich Transcriptional Profiling of <named-content content-type="genus-species">Staphylococcus aureus</named-content> During Growth in 2 M NaCl Leads to Clarification of Physiological Roles for Kdp and Ktr K<sup>+</sup> Uptake Systems
description	ABSTRACT Staphylococcus aureus exhibits an unusually high level of osmotolerance and Na+ tolerance, properties that support survival in various host niches and in preserved foods. The genetic basis of these traits is not well understood. We compared the transcriptional profiles of S. aureus grown in complex medium with and without 2 M NaCl. The stimulon for growth in high-osmolality media and Na+ included genes involved in uptake of K+, other compatible solutes, sialic acid, and sugars; capsule biosynthesis; and amino acid and central metabolism. Quantitative PCR analysis revealed that the loci responded differently from each other to high osmolality imposed by elevated NaCl versus sucrose. High-affinity K+ uptake (kdp) genes and capsule biosynthesis (cap5) genes required the two-component system KdpDE for full induction by osmotic stress, with kdpA induced more by NaCl and cap5B induced more by sucrose. Focusing on K+ importers, we identified three S. aureus genes belonging to the lower-affinity Trk/Ktr family that encode two membrane proteins (KtrB and KtrD) and one accessory protein (KtrC). In the absence of osmotic stress, the ktr gene transcripts were much more abundant than the kdpA transcript. Disruption of S. aureus kdpA caused a growth defect under low-K+ conditions, disruption of ktrC resulted in a significant defect in 2 M NaCl, and a ΔktrC ΔkdpA double mutant exhibited both phenotypes. Protective effects of S. aureus Ktr transporters at elevated NaCl are consistent with previous indications that both Na+ and osmolality challenges are mitigated by the maintenance of a high cytoplasmic K+ concentration. IMPORTANCE There is general agreement that the osmotolerance and Na+ tolerance of Staphylococcus aureus are unusually high for a nonhalophile and support its capacity for human colonization, pathogenesis, and growth in food. Nonetheless, the molecular basis for these properties is not well defined. The genome-wide response of S. aureus to a high concentration, 2 M, of NaCl revealed the upregulation of expected genes, such as those for transporters of compatible solutes that are widely implicated in supporting osmotolerance. A high-affinity potassium uptake system, KdpFABC, was upregulated, although it generally plays a physiological role under very low K+ conditions. At higher K+ concentrations, a lower-affinity and more highly expressed type of K+ transporter system, Ktr transporters, was shown to play a significant role in high Na+ tolerance. This study illustrates the importance of the K+ status of the cell for tolerance of Na+ by S. aureus and underscores the importance of monovalent cation cycles in this pathogen.
format	article
author	Alexa Price-Whelan Chun Kit Poon Meredith A. Benson Tess T. Eidem Christelle M. Roux Jeffrey M. Boyd Paul M. Dunman Victor J. Torres Terry A. Krulwich
author_facet	Alexa Price-Whelan Chun Kit Poon Meredith A. Benson Tess T. Eidem Christelle M. Roux Jeffrey M. Boyd Paul M. Dunman Victor J. Torres Terry A. Krulwich
author_sort	Alexa Price-Whelan
title	Transcriptional Profiling of <named-content content-type="genus-species">Staphylococcus aureus</named-content> During Growth in 2 M NaCl Leads to Clarification of Physiological Roles for Kdp and Ktr K<sup>+</sup> Uptake Systems
title_short	Transcriptional Profiling of <named-content content-type="genus-species">Staphylococcus aureus</named-content> During Growth in 2 M NaCl Leads to Clarification of Physiological Roles for Kdp and Ktr K<sup>+</sup> Uptake Systems
title_full	Transcriptional Profiling of <named-content content-type="genus-species">Staphylococcus aureus</named-content> During Growth in 2 M NaCl Leads to Clarification of Physiological Roles for Kdp and Ktr K<sup>+</sup> Uptake Systems
title_fullStr	Transcriptional Profiling of <named-content content-type="genus-species">Staphylococcus aureus</named-content> During Growth in 2 M NaCl Leads to Clarification of Physiological Roles for Kdp and Ktr K<sup>+</sup> Uptake Systems
title_full_unstemmed	Transcriptional Profiling of <named-content content-type="genus-species">Staphylococcus aureus</named-content> During Growth in 2 M NaCl Leads to Clarification of Physiological Roles for Kdp and Ktr K<sup>+</sup> Uptake Systems
title_sort	transcriptional profiling of <named-content content-type="genus-species">staphylococcus aureus</named-content> during growth in 2 m nacl leads to clarification of physiological roles for kdp and ktr k<sup>+</sup> uptake systems
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/9b4328fbcb9c4b819ce98ffec2f6dcef
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Transcriptional Profiling of <named-content content-type="genus-species">Staphylococcus aureus</named-content> During Growth in 2 M NaCl Leads to Clarification of Physiological Roles for Kdp and Ktr K<sup>+</sup> Uptake Systems

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