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Staphylococcus aureus Modulates Carotenoid and Phospholipid Content in Response to Oxygen-Restricted Growth Conditions, Triggering Changes in Membrane Biophysical Properties

Staphylococcus aureus membranes contain carotenoids formed during the biosynthesis of staphyloxanthin. These carotenoids are considered virulence factors due to their activity as scavengers of reactive oxygen species and as inhibitors of antimicrobial peptides. Here, we show that the growth of S. au...

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Autores principales: Zamudio-Chávez, Laura, Suesca, Elizabeth, López, Gerson-Dirceu, Carazzone, Chiara, Manrique-Moreno, Marcela, Leidy, Chad
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10573160/
https://www.ncbi.nlm.nih.gov/pubmed/37834354
http://dx.doi.org/10.3390/ijms241914906
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author Zamudio-Chávez, Laura
Suesca, Elizabeth
López, Gerson-Dirceu
Carazzone, Chiara
Manrique-Moreno, Marcela
Leidy, Chad
author_facet Zamudio-Chávez, Laura
Suesca, Elizabeth
López, Gerson-Dirceu
Carazzone, Chiara
Manrique-Moreno, Marcela
Leidy, Chad
author_sort Zamudio-Chávez, Laura
collection PubMed
description Staphylococcus aureus membranes contain carotenoids formed during the biosynthesis of staphyloxanthin. These carotenoids are considered virulence factors due to their activity as scavengers of reactive oxygen species and as inhibitors of antimicrobial peptides. Here, we show that the growth of S. aureus under oxygen-restricting conditions downregulates carotenoid biosynthesis and modifies phospholipid content in biofilms and planktonic cells analyzed using LC-MS. At oxygen-restrictive levels, the staphyloxanthin precursor 4,4-diapophytofluene accumulates, indicating that the dehydrogenation reaction catalyzed by 4,4′-diapophytoene desaturases (CrtN) is inhibited. An increase in lysyl-phosphatidylglycerol is observed under oxygen-restrictive conditions in planktonic cells, and high levels of cardiolipin are detected in biofilms compared to planktonic cells. Under oxygen-restriction conditions, the biophysical parameters of S. aureus membranes show an increase in lipid headgroup spacing, as measured with Laurdan GP, and decreased bilayer core order, as measured with DPH anisotropy. An increase in the liquid–crystalline to gel phase melting temperature, as measured with FTIR, is also observed. S. aureus membranes are therefore less condensed under oxygen-restriction conditions at 37 °C. However, the lack of carotenoids leads to a highly ordered gel phase at low temperatures, around 15 °C. Carotenoids are therefore likely to be low in S. aureus found in tissues with low oxygen levels, such as abscesses, leading to altered membrane biophysical properties.
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spelling pubmed-105731602023-10-14 Staphylococcus aureus Modulates Carotenoid and Phospholipid Content in Response to Oxygen-Restricted Growth Conditions, Triggering Changes in Membrane Biophysical Properties Zamudio-Chávez, Laura Suesca, Elizabeth López, Gerson-Dirceu Carazzone, Chiara Manrique-Moreno, Marcela Leidy, Chad Int J Mol Sci Article Staphylococcus aureus membranes contain carotenoids formed during the biosynthesis of staphyloxanthin. These carotenoids are considered virulence factors due to their activity as scavengers of reactive oxygen species and as inhibitors of antimicrobial peptides. Here, we show that the growth of S. aureus under oxygen-restricting conditions downregulates carotenoid biosynthesis and modifies phospholipid content in biofilms and planktonic cells analyzed using LC-MS. At oxygen-restrictive levels, the staphyloxanthin precursor 4,4-diapophytofluene accumulates, indicating that the dehydrogenation reaction catalyzed by 4,4′-diapophytoene desaturases (CrtN) is inhibited. An increase in lysyl-phosphatidylglycerol is observed under oxygen-restrictive conditions in planktonic cells, and high levels of cardiolipin are detected in biofilms compared to planktonic cells. Under oxygen-restriction conditions, the biophysical parameters of S. aureus membranes show an increase in lipid headgroup spacing, as measured with Laurdan GP, and decreased bilayer core order, as measured with DPH anisotropy. An increase in the liquid–crystalline to gel phase melting temperature, as measured with FTIR, is also observed. S. aureus membranes are therefore less condensed under oxygen-restriction conditions at 37 °C. However, the lack of carotenoids leads to a highly ordered gel phase at low temperatures, around 15 °C. Carotenoids are therefore likely to be low in S. aureus found in tissues with low oxygen levels, such as abscesses, leading to altered membrane biophysical properties. MDPI 2023-10-05 /pmc/articles/PMC10573160/ /pubmed/37834354 http://dx.doi.org/10.3390/ijms241914906 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Zamudio-Chávez, Laura
Suesca, Elizabeth
López, Gerson-Dirceu
Carazzone, Chiara
Manrique-Moreno, Marcela
Leidy, Chad
Staphylococcus aureus Modulates Carotenoid and Phospholipid Content in Response to Oxygen-Restricted Growth Conditions, Triggering Changes in Membrane Biophysical Properties
title Staphylococcus aureus Modulates Carotenoid and Phospholipid Content in Response to Oxygen-Restricted Growth Conditions, Triggering Changes in Membrane Biophysical Properties
title_full Staphylococcus aureus Modulates Carotenoid and Phospholipid Content in Response to Oxygen-Restricted Growth Conditions, Triggering Changes in Membrane Biophysical Properties
title_fullStr Staphylococcus aureus Modulates Carotenoid and Phospholipid Content in Response to Oxygen-Restricted Growth Conditions, Triggering Changes in Membrane Biophysical Properties
title_full_unstemmed Staphylococcus aureus Modulates Carotenoid and Phospholipid Content in Response to Oxygen-Restricted Growth Conditions, Triggering Changes in Membrane Biophysical Properties
title_short Staphylococcus aureus Modulates Carotenoid and Phospholipid Content in Response to Oxygen-Restricted Growth Conditions, Triggering Changes in Membrane Biophysical Properties
title_sort staphylococcus aureus modulates carotenoid and phospholipid content in response to oxygen-restricted growth conditions, triggering changes in membrane biophysical properties
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10573160/
https://www.ncbi.nlm.nih.gov/pubmed/37834354
http://dx.doi.org/10.3390/ijms241914906
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