Role of Staphyloxanthin in the lateral diffusion coefficient of a Staphylococcus aureus model membrane system
Lateral diffusion can be understood as the stochastic motion of microscopic molecules in a two-dimensional surface. The associated lateral diffusion coefficient gives the amount of area covered by a particle moving in lateral diffusion in a determined time. In biological sciences, this coefficient g...
- Autores:
-
Sandoval Granados, Juan Esteban
- Tipo de recurso:
- Trabajo de grado de pregrado
- Fecha de publicación:
- 2023
- Institución:
- Universidad de los Andes
- Repositorio:
- Séneca: repositorio Uniandes
- Idioma:
- eng
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- oai:repositorio.uniandes.edu.co:1992/73569
- Acceso en línea:
- https://hdl.handle.net/1992/73569
- Palabra clave:
- Membrane biophysics
Lateral diffusion
Staphylococcus aureus
Staphyloxanthin
Fluorescence correlation spectroscopy
Física
- Rights
- openAccess
- License
- Attribution-NoDerivatives 4.0 International
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dc.title.eng.fl_str_mv |
Role of Staphyloxanthin in the lateral diffusion coefficient of a Staphylococcus aureus model membrane system |
title |
Role of Staphyloxanthin in the lateral diffusion coefficient of a Staphylococcus aureus model membrane system |
spellingShingle |
Role of Staphyloxanthin in the lateral diffusion coefficient of a Staphylococcus aureus model membrane system Membrane biophysics Lateral diffusion Staphylococcus aureus Staphyloxanthin Fluorescence correlation spectroscopy Física |
title_short |
Role of Staphyloxanthin in the lateral diffusion coefficient of a Staphylococcus aureus model membrane system |
title_full |
Role of Staphyloxanthin in the lateral diffusion coefficient of a Staphylococcus aureus model membrane system |
title_fullStr |
Role of Staphyloxanthin in the lateral diffusion coefficient of a Staphylococcus aureus model membrane system |
title_full_unstemmed |
Role of Staphyloxanthin in the lateral diffusion coefficient of a Staphylococcus aureus model membrane system |
title_sort |
Role of Staphyloxanthin in the lateral diffusion coefficient of a Staphylococcus aureus model membrane system |
dc.creator.fl_str_mv |
Sandoval Granados, Juan Esteban |
dc.contributor.advisor.none.fl_str_mv |
Rey Suárez, Iván Adolfo Leidy, Chad |
dc.contributor.author.none.fl_str_mv |
Sandoval Granados, Juan Esteban |
dc.contributor.jury.none.fl_str_mv |
Aponte SantaMaría, Camilo Andrés |
dc.contributor.researchgroup.none.fl_str_mv |
Facultad de Ciencias::Biofísica |
dc.subject.keyword.eng.fl_str_mv |
Membrane biophysics Lateral diffusion Staphylococcus aureus Staphyloxanthin Fluorescence correlation spectroscopy |
topic |
Membrane biophysics Lateral diffusion Staphylococcus aureus Staphyloxanthin Fluorescence correlation spectroscopy Física |
dc.subject.themes.spa.fl_str_mv |
Física |
description |
Lateral diffusion can be understood as the stochastic motion of microscopic molecules in a two-dimensional surface. The associated lateral diffusion coefficient gives the amount of area covered by a particle moving in lateral diffusion in a determined time. In biological sciences, this coefficient gives insights into the molecular dynamics of cells and their interaction with biomolecules such as proteins and enzymes. Furthermore, Staphylococcus aureus (abbreviated as S. aureus ) is one of the most relevant bacteria due to its large incidence of respiratory infections and its resistance to multiple commercial antibiotics. Among S. aureus defense mechanisms, Staphyloxanthin (STX) stands out as a carotenoid molecule capable of stopping oxidation processes in S. aureus membrane in high-stress conditions. In previous literature, the effects of STX in different biophysical properties of S. aureus membrane such as rigidity and elastic bending constant have been characterized; however, the effect of STX in the lateral diffusion coefficient of S. aureus membrane still remains unknown. In this work, we characterize the Fluorescence Correlation Spectroscopy (FCS) technique to measure lateral diffusion coefficients in biological membranes by the autocorrelation function associated to the measured membrane fluorescence signal in a confocal microscope. By using this technique, we successfully measured the lateral diffusion coefficient of giant unilamellar vesicles (GUVs) made of the lipid DOPC along with the lipophillic fluorophore DiI at 37°C and 45◦C, corroborating the effect of temperature in diffusion dynamics. Additionally, we observed the effects of STX (15mol%) in the lateral diffusion coefficient of S. aureus model membrane GUVs made of the lipids DMPC (85mol%), DMPG (15mol%) and DiI. The presence of STX increases the lateral diffusion coefficient by almost 2^2/ when compared to the case without STX at 37°C. These results are expected to expand the knowledge on the biophysical properties of S. aureus and give additional insights into the possible ways to treat S. aureus infections without the use of antibiotics. |
publishDate |
2023 |
dc.date.issued.none.fl_str_mv |
2023-12-07 |
dc.date.accessioned.none.fl_str_mv |
2024-01-29T19:27:11Z |
dc.date.available.none.fl_str_mv |
2024-01-29T19:27:11Z |
dc.type.none.fl_str_mv |
Trabajo de grado - Pregrado |
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info:eu-repo/semantics/bachelorThesis |
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info:eu-repo/semantics/acceptedVersion |
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http://purl.org/coar/resource_type/c_7a1f |
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http://purl.org/redcol/resource_type/TP |
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https://hdl.handle.net/1992/73569 |
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instname:Universidad de los Andes |
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reponame:Repositorio Institucional Séneca |
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repourl:https://repositorio.uniandes.edu.co/ |
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identifier_str_mv |
instname:Universidad de los Andes reponame:Repositorio Institucional Séneca repourl:https://repositorio.uniandes.edu.co/ |
dc.language.iso.none.fl_str_mv |
eng |
language |
eng |
dc.relation.references.none.fl_str_mv |
Braungardt, H. & Singh, V. K. Impact of Deficiencies in Branched-Chain Fatty Acids and Staphyloxanthin in Staphylococcus aureus. BioMed Research International 2019, 1–8. issn: 2314-6133, 2314-6141 (Jan. 2019). Valderrama-Beltrán, S. et al. Risk factors associated with methicillin-resistant Staphylococcus aureus skin and soft tissue infections in hospitalized patients in Colombia. International Journal of Infectious Diseases 87, 60–66. issn: 1201-9712 (Oct. 2019). Chambers, H. F. & DeLeo, F. R. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nature Reviews Microbiology 7, 629–641. issn: 1740-1534 (Sept. 2009). Zouhir, A., Jridi, T., Nefzi, A., Ben Hamida, J. & Sebei, K. Inhibition of methicillin-resistant Staphylococcus aureus (MRSA) by antimicrobial peptides (AMPs) and plant essential oils. Pharmaceutical Biology 54, 3136–3150. issn: 1388-0209 (Dec. 2016). López, G.-D. et al. Carotenogenesis of Staphylococcus aureus: New insights and impact on membrane biophysical properties. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids 1866, 158941. issn: 1388-1981 (Aug. 2021). Xue, L. et al. Staphyloxanthin: a potential target for antivirulence therapy. Infection and Drug Resistance 12, 2151–2160 (July 2019). Perez-Lopez, M. I. et al. Variations in carotenoid content and acyl chain composition in exponential, stationary and biofilm states of Staphylococcus aureus, and their influence on membrane biophysical properties. Biochimica et Biophysica Acta (BBA) - Biomembranes 1861, 978–987. issn: 0005-2736 (May 2019). Sekimoto, K. Stochastic Energetics isbn: 978-3-642-05410-5. https://link.springer.com/10.1007/978-3-642-05411-2 (Springer, Berlin, Heidelberg, 2010). Heimburg, T. Thermal Biophysics of Membranes isbn: 978-3-527-40471-1. https://onlinelibrary.wiley.com/doi/book/10.1002/9783527611591 (Wiley-VCH, July 2007). Kang, M., Day, C. A., Kenworthy, A. K. & DiBenedetto, E. Simplified equation to extract diffusion coefficients from confocal FRAP data. eng. 13, 1589–1600. issn: 1600-0854 (Dec. 2012). Shen, H.et al. Single Particle Tracking: From Theory to Biophysical Applications. Chemical Reviews 117, 7331–7376. issn: 0009-2665 (June 2017). Yu, L. et al. A Comprehensive Review of Fluorescence Correlation Spectroscopy. Frontiers in Physics 9. issn: 2296-424X. https://www.frontiersin.org/articles/10.3389/fphy.2021.644450 (2021). Schwille, P., Korlach, J. & Webb, W. W. Fluorescence correlation spectroscopy with single-molecule sensitivity on cell and model membranes. Cytometry 36, 176–182. issn: 0196-4763 (July 1999). Macháň, R. & Hof, M. Recent Developments in Fluorescence Correlation Spectroscopy for Diffusion Measurements in Planar Lipid Membranes. International Journal of Molecular Sciences 11, 427–457. issn: 1422-0067 (Feb. 2010). Elson, E. L. & Magde, D. Fluorescence correlation spectroscopy. I. Conceptual basis and theory. Biopolymers 13, 1–27. issn: 1097-0282 (1974). Rey-Suárez, I., Leidy, C., Téllez, G., Gay, G. & Gonzalez-Mancera, A. Slow Sedimentation and Deformability of Charged Lipid Vesicles. PLOS ONE 8, e68309. issn: 1932-6203 (July 2013). Pereno, V. et al. Electroformation of Giant Unilamellar Vesicles on Stainless Steel Elec trodes. ACS Omega 2, 994–1002 (Mar. 2017). Méléard, P., Bagatolli, L. A. & Pott, T. in Methods in Enzymology 161–176 (Academic Press, June 2009). https://www.sciencedirect.com/science/article/pii/S0076687909650096. Alberts, B. et al. Molecular Biology of the Cell, 5th Edition 74–75. isbn: 978-0-8153-4105-5 (New York, Nov. 2007). Windmaier, E., Raff, H. & Strang, K. in Vander’s human physiology: the mechanisms of body function Fourteenth edition, 138–173 (McGraw-Hill Education, New York, 2016). isbn: 978-1-259-29409-9. Nelson, D. L. & Cox, M. M. in Lehninger Principles of Biochemistry 4th ed., 348–355 (New York, Nov. 2012). isbn: 978-1-4292-3414-6. Chan, Y.-H. M. & Boxer, S. G. Model Membrane Systems and Their Applications. Current opinion in chemical biology 11, 581–587. issn: 1367-5931 (Dec. 2007). Richter, R. P., Bérat, R. & Brisson, A. R. Formation of Solid-Supported Lipid Bilayers: An Integrated View. Langmuir 22, 3497–3505. issn: 0743-7463 (Apr. 2006). Tong, S. Y. C., Davis, J. S., Eichenberger, E., Holland, T. L. & Fowler, V. G. Staphylo coccus aureus Infections: Epidemiology, Pathophysiology, Clinical Manifestations, and Management. Clinical Microbiology Reviews 28, 603–661. issn: 0893-8512 (July 2015). Rasigade, J.-P. & Vandenesch, F. Staphylococcus aureus: a pathogen with still unre solved issues. eng. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases 21, 510–514. issn: 1567-7257 (Jan. 2014). Zamudio-Chávez, L. et al. Staphylococcus aureus Modulates Carotenoid and Phospho lipid Content in Response to Oxygen-Restricted Growth Conditions, Triggering Changes in Membrane Biophysical Properties. International Journal of Molecular Sciences 24, 14906. issn: 1422-0067 (Jan. 2023). Elmesseri, R. A., Saleh, S. E., Elsherif, H. M., Yahia, I. S. & Aboshanab, K. M. Staphy loxanthin as a Potential Novel Target for Deciphering Promising Anti-Staphylococcus aureus Agents. Antibiotics 11, 298. issn: 2079-6382 (Feb. 2022). Shai, Y. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by -helical antimicrobial and cell non-selective membrane-lytic peptides. Biochimica et Biophysica Acta (BBA) - Biomembranes 1462, 55–70. issn: 0005-2736 (Dec. 1999). Pathria, R. K. & Beale, P. D. in Statistical Mechanics (Third Edition) (eds Pathria, R. K. & Beale, P. D.) 583–635 (Academic Press, Boston, Jan. 2011). isbn: 978-0-12-382188-1. https://www.sciencedirect.com/science/article/pii/B9780123821881000153. Smith-Dupont, K. B., Guo, L. & Gai, F. Diffusion as a Probe of the Heterogeneity of Antimicrobial Peptide - Membrane Interactions. Biochemistry 49, 4672–4678. issn: 0006-2960 (Nov. 2010). Ramadurai, S. et al. Lateral Diffusion of Membrane Proteins. Journal of the American Chemical Society 131, 12650–12656. issn: 0002-7863 (Sept. 2009). Waithe, D. et al. Optimized processing and analysis of conventional confocal microscopy generated scanning FCS data. Methods. Developments in Fluorescence Correlation Spec troscopy and related techniques 140–141, 62–73. issn: 1046-2023 (May 2018). Macháň, R. & Hof, M. in. Chap. 5 (). https://tinyurl.com/bdcwsejh. Ross, S. M. in Introduction to Probability and Statistics for Engineers and Scientists (Fifth Edition) (ed Ross, S. M.) 9–51 (Academic Press, Boston, Jan. 2014). isbn: 978-0-12-394811-3. https://www.sciencedirect.com/science/article/pii/B9780123948113500022. Nwaneshiudu, A. et al. Introduction to confocal microscopy. Journal of Investigative Dermatology 132, 1–5. issn: 0022-202X (Dec. 2012). Drabik, D., Doskocz, J. & Przybyło, M. Effects of electroformation protocol parameters on quality of homogeneous GUV populations. 212, 88–95. issn: 0009-3084 (May 2018). Menger, F. M. & Angelova, M. I. Giant Vesicles: Imitating the Cytological Processes of Cell Membranes. Accounts of Chemical Research 31, 789–797. issn: 0001-4842 (Dec. 1998). Jan Akhunzada, M. et al. Interplay between lipid lateral diffusion, dye concentration and membrane permeability unveiled by a combined spectroscopic and computational study of a model lipid bilayer. Scientific Reports 9, 1508. issn: 2045-2322 (Feb. 2019). Guo, L.et al. Molecular Diffusion Measurement in Lipid Bilayers over Wide Concentration Ranges: A Comparative Study. ChemPhysChem 9, 721–728. issn: 1439-7641 (2008). Lewis, R. N. A. H., Zhang, Y.-P. & McElhaney, R. N. Calorimetric and spectroscopic studies of the phase behavior and organization of lipid bilayer model membranes composed of binary mixtures of dimyristoylphosphatidylcholine and dimyristoylphosphatidylglycerol. Biochimica et Biophysica Acta (BBA) - Biomembranes 1668, 203–214. issn: 0005-2736 (Mar. 2005). Leidy, C., Wolkers, W. F., Jørgensen, K., Mouritsen, O. G. & Crowe, J. H. Lateral Organization and Domain Formation in a Two-Component Lipid Membrane System. Biophysical Journal 80, 1819–1828. issn: 00063495 (Apr. 2001). Múnera-Jaramillo, J. et al. The Role of Staphyloxanthin in the Regulation of Membrane Biophysical Properties in Staphylococcus aureus. To be published. |
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Rey Suárez, Iván AdolfoLeidy, Chadvirtual::186-1Sandoval Granados, Juan EstebanAponte SantaMaría, Camilo Andrésvirtual::187-1Facultad de Ciencias::Biofísica2024-01-29T19:27:11Z2024-01-29T19:27:11Z2023-12-07https://hdl.handle.net/1992/73569instname:Universidad de los Andesreponame:Repositorio Institucional Sénecarepourl:https://repositorio.uniandes.edu.co/Lateral diffusion can be understood as the stochastic motion of microscopic molecules in a two-dimensional surface. The associated lateral diffusion coefficient gives the amount of area covered by a particle moving in lateral diffusion in a determined time. In biological sciences, this coefficient gives insights into the molecular dynamics of cells and their interaction with biomolecules such as proteins and enzymes. Furthermore, Staphylococcus aureus (abbreviated as S. aureus ) is one of the most relevant bacteria due to its large incidence of respiratory infections and its resistance to multiple commercial antibiotics. Among S. aureus defense mechanisms, Staphyloxanthin (STX) stands out as a carotenoid molecule capable of stopping oxidation processes in S. aureus membrane in high-stress conditions. In previous literature, the effects of STX in different biophysical properties of S. aureus membrane such as rigidity and elastic bending constant have been characterized; however, the effect of STX in the lateral diffusion coefficient of S. aureus membrane still remains unknown. In this work, we characterize the Fluorescence Correlation Spectroscopy (FCS) technique to measure lateral diffusion coefficients in biological membranes by the autocorrelation function associated to the measured membrane fluorescence signal in a confocal microscope. By using this technique, we successfully measured the lateral diffusion coefficient of giant unilamellar vesicles (GUVs) made of the lipid DOPC along with the lipophillic fluorophore DiI at 37°C and 45◦C, corroborating the effect of temperature in diffusion dynamics. Additionally, we observed the effects of STX (15mol%) in the lateral diffusion coefficient of S. aureus model membrane GUVs made of the lipids DMPC (85mol%), DMPG (15mol%) and DiI. The presence of STX increases the lateral diffusion coefficient by almost 2^2/ when compared to the case without STX at 37°C. These results are expected to expand the knowledge on the biophysical properties of S. aureus and give additional insights into the possible ways to treat S. aureus infections without the use of antibiotics.FísicoPregradoBiofísica de membranas41 páginasapplication/pdfengUniversidad de los AndesFísicaFacultad de CienciasDepartamento de FísicaAttribution-NoDerivatives 4.0 Internationalhttp://creativecommons.org/licenses/by-nd/4.0/info:eu-repo/semantics/openAccesshttp://purl.org/coar/access_right/c_abf2Role of Staphyloxanthin in the lateral diffusion coefficient of a Staphylococcus aureus model membrane systemTrabajo de grado - Pregradoinfo:eu-repo/semantics/bachelorThesisinfo:eu-repo/semantics/acceptedVersionhttp://purl.org/coar/resource_type/c_7a1fTexthttp://purl.org/redcol/resource_type/TPMembrane biophysicsLateral diffusionStaphylococcus aureusStaphyloxanthinFluorescence correlation spectroscopyFísicaBraungardt, H. & Singh, V. K. Impact of Deficiencies in Branched-Chain Fatty Acids and Staphyloxanthin in Staphylococcus aureus. BioMed Research International 2019, 1–8. issn: 2314-6133, 2314-6141 (Jan. 2019).Valderrama-Beltrán, S. et al. Risk factors associated with methicillin-resistant Staphylococcus aureus skin and soft tissue infections in hospitalized patients in Colombia. International Journal of Infectious Diseases 87, 60–66. issn: 1201-9712 (Oct. 2019).Chambers, H. F. & DeLeo, F. R. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nature Reviews Microbiology 7, 629–641. issn: 1740-1534 (Sept. 2009).Zouhir, A., Jridi, T., Nefzi, A., Ben Hamida, J. & Sebei, K. Inhibition of methicillin-resistant Staphylococcus aureus (MRSA) by antimicrobial peptides (AMPs) and plant essential oils. Pharmaceutical Biology 54, 3136–3150. issn: 1388-0209 (Dec. 2016).López, G.-D. et al. Carotenogenesis of Staphylococcus aureus: New insights and impact on membrane biophysical properties. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids 1866, 158941. issn: 1388-1981 (Aug. 2021).Xue, L. et al. Staphyloxanthin: a potential target for antivirulence therapy. Infection and Drug Resistance 12, 2151–2160 (July 2019).Perez-Lopez, M. I. et al. Variations in carotenoid content and acyl chain composition in exponential, stationary and biofilm states of Staphylococcus aureus, and their influence on membrane biophysical properties. Biochimica et Biophysica Acta (BBA) - Biomembranes 1861, 978–987. issn: 0005-2736 (May 2019).Sekimoto, K. Stochastic Energetics isbn: 978-3-642-05410-5. https://link.springer.com/10.1007/978-3-642-05411-2 (Springer, Berlin, Heidelberg, 2010).Heimburg, T. Thermal Biophysics of Membranes isbn: 978-3-527-40471-1. https://onlinelibrary.wiley.com/doi/book/10.1002/9783527611591 (Wiley-VCH, July 2007).Kang, M., Day, C. A., Kenworthy, A. K. & DiBenedetto, E. Simplified equation to extract diffusion coefficients from confocal FRAP data. eng. 13, 1589–1600. issn: 1600-0854 (Dec. 2012).Shen, H.et al. Single Particle Tracking: From Theory to Biophysical Applications. Chemical Reviews 117, 7331–7376. issn: 0009-2665 (June 2017).Yu, L. et al. A Comprehensive Review of Fluorescence Correlation Spectroscopy. Frontiers in Physics 9. issn: 2296-424X. https://www.frontiersin.org/articles/10.3389/fphy.2021.644450 (2021).Schwille, P., Korlach, J. & Webb, W. W. Fluorescence correlation spectroscopy with single-molecule sensitivity on cell and model membranes. Cytometry 36, 176–182. issn: 0196-4763 (July 1999).Macháň, R. & Hof, M. Recent Developments in Fluorescence Correlation Spectroscopy for Diffusion Measurements in Planar Lipid Membranes. International Journal of Molecular Sciences 11, 427–457. issn: 1422-0067 (Feb. 2010).Elson, E. L. & Magde, D. Fluorescence correlation spectroscopy. I. Conceptual basis and theory. Biopolymers 13, 1–27. issn: 1097-0282 (1974).Rey-Suárez, I., Leidy, C., Téllez, G., Gay, G. & Gonzalez-Mancera, A. Slow Sedimentation and Deformability of Charged Lipid Vesicles. PLOS ONE 8, e68309. issn: 1932-6203 (July 2013).Pereno, V. et al. Electroformation of Giant Unilamellar Vesicles on Stainless Steel Elec trodes. ACS Omega 2, 994–1002 (Mar. 2017).Méléard, P., Bagatolli, L. A. & Pott, T. in Methods in Enzymology 161–176 (Academic Press, June 2009). https://www.sciencedirect.com/science/article/pii/S0076687909650096.Alberts, B. et al. Molecular Biology of the Cell, 5th Edition 74–75. isbn: 978-0-8153-4105-5 (New York, Nov. 2007).Windmaier, E., Raff, H. & Strang, K. in Vander’s human physiology: the mechanisms of body function Fourteenth edition, 138–173 (McGraw-Hill Education, New York, 2016). isbn: 978-1-259-29409-9.Nelson, D. L. & Cox, M. M. in Lehninger Principles of Biochemistry 4th ed., 348–355 (New York, Nov. 2012). isbn: 978-1-4292-3414-6.Chan, Y.-H. M. & Boxer, S. G. Model Membrane Systems and Their Applications. Current opinion in chemical biology 11, 581–587. issn: 1367-5931 (Dec. 2007).Richter, R. P., Bérat, R. & Brisson, A. R. Formation of Solid-Supported Lipid Bilayers: An Integrated View. Langmuir 22, 3497–3505. issn: 0743-7463 (Apr. 2006).Tong, S. Y. C., Davis, J. S., Eichenberger, E., Holland, T. L. & Fowler, V. G. Staphylo coccus aureus Infections: Epidemiology, Pathophysiology, Clinical Manifestations, and Management. Clinical Microbiology Reviews 28, 603–661. issn: 0893-8512 (July 2015).Rasigade, J.-P. & Vandenesch, F. Staphylococcus aureus: a pathogen with still unre solved issues. eng. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases 21, 510–514. issn: 1567-7257 (Jan. 2014).Zamudio-Chávez, L. et al. Staphylococcus aureus Modulates Carotenoid and Phospho lipid Content in Response to Oxygen-Restricted Growth Conditions, Triggering Changes in Membrane Biophysical Properties. International Journal of Molecular Sciences 24, 14906. issn: 1422-0067 (Jan. 2023).Elmesseri, R. A., Saleh, S. E., Elsherif, H. M., Yahia, I. S. & Aboshanab, K. M. Staphy loxanthin as a Potential Novel Target for Deciphering Promising Anti-Staphylococcus aureus Agents. Antibiotics 11, 298. issn: 2079-6382 (Feb. 2022).Shai, Y. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by -helical antimicrobial and cell non-selective membrane-lytic peptides. Biochimica et Biophysica Acta (BBA) - Biomembranes 1462, 55–70. issn: 0005-2736 (Dec. 1999).Pathria, R. K. & Beale, P. D. in Statistical Mechanics (Third Edition) (eds Pathria, R. K. & Beale, P. 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