Identification of staphyloxanthin and derivates in yellow-pigmented Staphylococcus capitis subsp. capitis
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
37840735
PubMed Central
PMC10570620
DOI
10.3389/fmicb.2023.1272734
Knihovny.cz E-zdroje
- Klíčová slova
- Staphylococcus capitis, bacterial pigments, carotenoids, coagulase-negative staphylococci (CoNS), staphyloxanthin,
- Publikační typ
- časopisecké články MeSH
INTRODUCTION: Staphylococcus capitis naturally colonizes the human skin but as an opportunistic pathogen, it can also cause biofilm-associated infections and bloodstream infections in newborns. Previously, we found that two strains from the subspecies S. capitis subsp. capitis produce yellow carotenoids despite the initial species description, reporting this subspecies as non-pigmented. In Staphylococcus aureus, the golden pigment staphyloxanthin is an important virulence factor, protecting cells against reactive oxygen species and modulating membrane fluidity. METHODS: In this study, we used two pigmented (DSM 111179 and DSM 113836) and two non-pigmented S. capitis subsp. capitis strains (DSM 20326T and DSM 31028) to identify the pigment, determine conditions under which pigment-production occurs and investigate whether pigmented strains show increased resistance to ROS and temperature stress. RESULTS: We found that the non-pigmented strains remained colorless regardless of the type of medium, whereas intensity of pigmentation in the two pigmented strains increased under low nutrient conditions and with longer incubation times. We were able to detect and identify staphyloxanthin and its derivates in the two pigmented strains but found that methanol cell extracts from all four strains showed ROS scavenging activity regardless of staphyloxanthin production. Increased survival to cold temperatures (-20°C) was detected in the two pigmented strains only after long-term storage compared to the non-pigmented strains. CONCLUSION: The identification of staphyloxanthin in S. capitis is of clinical relevance and could be used, in the same way as in S. aureus, as a possible target for anti-virulence drug design.
Department of Algorithmic Bioinformatics Justus Liebig University Giessen Giessen Germany
Department of Bioinformatics and Systems Biology Justus Liebig University Giessen Giessen Germany
Institute of Nutritional and Food Sciences Food Sciences University of Bonn Bonn Germany
Institute of Scientific Instruments of the Czech Academy of Sciences Brno Czechia
Zobrazit více v PubMed
Asker D., Beppu T., Ueda K. (2007). Unique diversity of carotenoid-producing bacteria isolated from Misasa, a radioactive site in Japan. Appl. Microbiol. Biotechnol. 77, 383–392. doi: 10.1007/s00253-007-1157-8, PMID: PubMed DOI
Ayala O. D., Wakeman C. A., Pence I. J., Gaddy J. A., Slaughter J. C., Skaar E. P., et al. . (2018). Drug-resistant Staphylococcus aureus strains reveal distinct biochemical features with Raman microspectroscopy. ACS Infect. Dis. 4, 1197–1210. doi: 10.1021/acsinfecdis.8b00029, PMID: PubMed DOI PMC
Bannerman T. L., Kloos W. E. (1991). Staphylococcus capitis subsp. ureolyticus subsp. nov. from human skin. Int. J. Syst. Bacteriol. 41, 144–147. doi: 10.1099/00207713-41-1-144, PMID: PubMed DOI
Beard-Pegler M. A., Stubbs E., Vickery A. M. (1988). Observations on the resistance to drying of staphylococcal strains. J. Med. Microbiol. 26, 251–255. doi: 10.1099/00222615-26-4-251, PMID: PubMed DOI
Bernatova S., Samek O., Pilat Z., Sery M., Jezek J., Jakl P., et al. . (2013). Following the mechanisms of bacteriostatic versus bactericidal action using Raman spectroscopy. Molecules 18, 13188–13199. doi: 10.3390/molecules181113188, PMID: PubMed DOI PMC
Breithaupt D. E., Schwack W., Wolf G., Hammes W. P. (2001). Characterization of the triterpenoid 4,4′-diaponeurosporene and its isomers in food-associated bacteria. Eur. Food Res. Technol. 213, 231–233. doi: 10.1007/s002170100358 DOI
Bull A. T. (1970). Inhibition of polysaccharases by melanin: enzyme inhibition in relation to mycolysis. Arch. Biochem. Biophys. 137, 345–356. doi: 10.1016/0003-9861(70)90448-0, PMID: PubMed DOI
Cameron D. R., Jiang J. H., Hassan K. A., Elbourne L. D., Tuck K. L., Paulsen I. T., et al. . (2015). Insights on virulence from the complete genome of Staphylococcus capitis. Front. Microbiol. 6:980. doi: 10.3389/fmicb.2015.00980, PMID: PubMed DOI PMC
Chong C. E., Bengtsson R. J., Horsburgh M. J. (2022). Comparative genomics of Staphylococcus capitis reveals species determinants. Front. Microbiol. 13:1005949. doi: 10.3389/fmicb.2022.1005949, PMID: PubMed DOI PMC
Clauditz A., Resch A., Wieland K. P., Peschel A., Götz F. (2006). Staphyloxanthin plays a role in the fitness of Staphylococcus aureus and its ability to cope with oxidative stress. Infect. Immun. 74, 4950–4953. doi: 10.1128/IAI.00204-06, PMID: PubMed DOI PMC
Cui B., Smooker P. M., Rouch D. A., Daley A. J., Deighton M. A. (2013). Differences between two clinical Staphylococcus capitis subspecies as revealed by biofilm, antibiotic resistance, and pulsed-field gel electrophoresis profiling. J. Clin. Microbiol. 51, 9–14. doi: 10.1128/JCM.05124-11, PMID: PubMed DOI PMC
De Maesschalck R., Jouan-Rimbaud D., Massart D. L. (2000). The Mahalanobis distance. Chemom. Intell. Lab. Syst. 50, 1–18. doi: 10.1016/S0169-7439(99)00047-7, PMID: PubMed DOI
Decalonne M., Dos Santos S., Gimenes R., Goube F., Abadie G., Aberrane S., et al. . (2020). Staphylococcus capitis isolated from bloodstream infections: a nationwide 3-month survey in 38 neonatal intensive care units. Eur. J. Clin. Microbiol. Infect. Dis. 39, 2185–2194. doi: 10.1007/s10096-020-03925-5, PMID: PubMed DOI PMC
Dieckmann M. A. B. S., Nkouamedjo-Fankep R. C., Hanel P. H. G., Jelonek L., Blom J., Goesmann A. (2021). EDGAR3.0: comparative genomics and phylogenomics on a scalable infrastructure. Nucleic Acids Res. 49, W185–W192. doi: 10.1093/nar/gkab341, PMID: PubMed DOI PMC
Dieser M., Greenwood M., Foreman C. M. (2010). Carotenoid pigmentation in Antarctic heterotrophic bacteria as a strategy to withstand environmental stresses. Arct. Antarct. Alp. Res. 42, 396–405. doi: 10.1657/1938-4246-42.4.396 DOI
Edgar R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797. doi: 10.1093/nar/gkh340, PMID: PubMed DOI PMC
El-Agamey A., Lowe G. M., McGarvey D. J., Mortensen A., Phillip D. M., Truscott T. G., et al. . (2004). Carotenoid radical chemistry and antioxidant/pro-oxidant properties. Arch. Biochem. Biophys. 430, 37–48. doi: 10.1016/j.abb.2004.03.007, PMID: PubMed DOI
Etzbach L., Pfeiffer A., Weber F., Schieber A. (2018). Characterization of carotenoid profiles in goldenberry (Physalis peruviana L.) fruits at various ripening stages and in different plant tissues by HPLC-DAD-APCI-MSn. Food Chem. 245, 508–517. doi: 10.1016/j.foodchem.2017.10.120 PubMed DOI
Fong N., Burgess M., Barrow K., Glenn D. (2001). Carotenoid accumulation in the psychrotrophic bacterium Arthrobacter agilis in response to thermal and salt stress. Appl. Microbiol. Biotechnol. 56, 750–756. doi: 10.1007/s002530100739 PubMed DOI
Gilchrist C. L. M., Chooi Y.-H. (2021). clinker & clustermap.js: automatic generation of gene cluster comparison figures. Bioinformatics 37, 2473–2475. doi: 10.1093/bioinformatics/btab007, PMID: PubMed DOI
Kaiser P., Surmann P., Vallentin G., Fuhrmann H. (2007). A small-scale method for quantitation of carotenoids in bacteria and yeasts. J. Microbiol. Methods 70, 142–149. doi: 10.1016/j.mimet.2007.04.004, PMID: PubMed DOI
Kim M., Jung D. H., Hwang C. Y., Siziya I. N., Park Y. S., Seo M. J. (2023). 4,4′-diaponeurosporene production as C30 carotenoid with antioxidant activity in recombinant Escherichia coli. Appl. Biochem. Biotechnol. 195, 135–151. doi: 10.1007/s12010-022-04147-5, PMID: PubMed DOI
Kim S. H., Kim M. S., Lee B. Y., Lee P. C. (2016). Generation of structurally novel short carotenoids and study of their biological activity. Sci. Rep. 6, 1–11. doi: 10.1038/srep21987, PMID: PubMed DOI PMC
Linden M., Flegler A., Feuereisen M. M., Weber F., Lipski A., Schieber A. (2023). Effects of flavonoids on membrane adaptation of food-associated bacteria. Biochim. Biophys. Acta 1865:184137. doi: 10.1016/j.bbamem.2023.184137, PMID: PubMed DOI
Liu G. Y., Essex A., Buchanan J. T., Datta V., Hoffman H. M., Bastian J. F., et al. . (2005). Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J. Exp. Med. 202, 209–215. doi: 10.1084/jem.20050846, PMID: PubMed DOI PMC
López G. D., Suesca E., Álvarez-Rivera G., Rosato A. E., Ibáñez E., Cifuentes A., et al. . (2021). Carotenogenesis of Staphylococcus aureus: new insights and impact on membrane biophysical properties. Biochim. Biophys. Acta 1866:158941. doi: 10.1016/j.bbalip.2021.158941, PMID: PubMed DOI
Madeira F., Pearce M., Tivey A. R. N., Basutkar P., Lee J., Edbali O., et al. . (2022). Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Res. 50, W276–W279. doi: 10.1093/nar/gkac240, PMID: PubMed DOI PMC
Marshall J. H., Wilmoth G. J. (1981). Pigments of Staphylococcus aureus, a series of triterpenoid carotenoids. J. Bacteriol. 147, 900–913. doi: 10.1128/jb.147.3.900-913.1981, PMID: PubMed DOI PMC
Merrikh C. N., Merrikh H. (2018). Gene inversion potentiates bacterial evolvability and virulence. Nat. Commun. 9:4662. doi: 10.1038/s41467-018-07110-3 PubMed DOI PMC
Mishra N. N., Liu G. Y., Yeaman M. R., Nast C. C., Proctor R. A., McKinnell J., et al. . (2011). Carotenoid-related alteration of cell membrane fluidity impacts Staphylococcus aureus susceptibility to host defense peptides. Antimicrob. Agents Chemother. 55, 526–531. doi: 10.1128/AAC.00680-10, PMID: PubMed DOI PMC
Mlynarikova K., Samek O., Bernatova S., Ruzicka F., Jezek J., Haronikova A., et al. . (2015). Influence of culture media on microbial fingerprints using Raman spectroscopy. Sensors 15, 29635–29647. doi: 10.3390/s151129635, PMID: PubMed DOI PMC
Moore J., Yu L. (2007). “Methods for antioxidant capacity estimation of wheat and wheat-based food products” in Wheat antioxidants. ed. Yu L. (Hoboken, New Jersey, United States: John Wiley & Sons, Inc.), 118–172.
Mora M., Wink L., Kögler I., Mahnert A., Rettberg P., Schwendner P., et al. . (2019). Space station conditions are selective but do not alter microbial characteristics relevant to human health. Nat. Commun. 10:3990. doi: 10.1038/s41467-019-11682-z PubMed DOI PMC
Natsis N. E., Cohen P. R. (2018). Coagulase-negative Staphylococcus skin and soft tissue infections. Am. J. Clin. Dermatol. 19, 671–677. doi: 10.1007/s40257-018-0362-9, PMID: PubMed DOI
Palma M., Cheung A. L. (2001). ςB activity in Staphylococcus aureus is controlled by RsbU and an additional factor(s) during bacterial growth. Infect. Immun. 69, 7858–7865. doi: 10.1128/IAI.69.12.7858-7865.2001, PMID: PubMed DOI PMC
Pannu M. K., Hudman D. A., Sargentini N. J., Singh V. K. (2019). Role of SigB and staphyloxanthin in radiation survival of Staphylococcus aureus. Curr. Microbiol. 76, 70–77. doi: 10.1007/s00284-018-1586-x, PMID: PubMed DOI
Pelz A., Wieland K.-P., Putzbach K., Hentschel P., Albert K., Götz F. (2005). Structure and biosynthesis of staphyloxanthin from Staphylococcus aureus. J. Biol. Chem. 280, 32493–32498. doi: 10.1074/jbc.M505070200, PMID: PubMed DOI
Rebrošová K., Šiler M., Samek O., Růžička F., Bernatová S., Ježek J., et al. . (2017). Differentiation between Staphylococcus aureus and Staphylococcus epidermidis strains using Raman spectroscopy. Future Microbiol. 12, 881–890. doi: 10.2217/fmb-2016-0224, PMID: PubMed DOI
Renishaw (2003). Technical note: Renishaw’s EasyConfocal Raman method SPD/TN/076. Wotton-under-Edge. Rehnishaw PLC
Sajjad W., Din G., Rafiq M., Iqbal A., Khan S., Zada S., et al. . (2020). Pigment production by cold-adapted bacteria and fungi: colorful tale of cryosphere with wide range applications. Extremophiles 24, 447–473. doi: 10.1007/s00792-020-01180-2, PMID: PubMed DOI PMC
Salamzade R., Cheong J. Z. A., Sandstrom S., Swaney M. H., Stubbendieck R. M., Starr N. L., et al. . (2023). Evolutionary investigations of the biosynthetic diversity in the skin microbiome using lsa BGC. Microb. Genom. 9:mgen000988. doi: 10.1099/mgen.0.000988, PMID: PubMed DOI PMC
Schwengers O., Jelonek L., Dieckmann M. A., Beyvers S., Blom J., Goesmann A. (2021). Bakta: rapid and standardized annotation of bacterial genomes via alignment-free sequence identification. Microb. Genom. 7:000685. doi: 10.1099/mgen.0.000685, PMID: PubMed DOI PMC
Seel W., Baust D., Sons D., Albers M., Etzbach L., Fuss J., et al. . (2020). Carotenoids are used as regulators for membrane fluidity by Staphylococcus xylosus. Sci. Rep. 10:330. doi: 10.1038/s41598-019-57006-5, PMID: PubMed DOI PMC
Sendra J. M., Sentandreu E., Navarro J. L. (2006). Reduction kinetics of the free stable radical 2,2-diphenyl-1-picrylhydrazyl (DPPH•) for determination of the antiradical activity of citrus juices. Eur. Food Res. Technol. 223:615. doi: 10.1007/s00217-005-0243-3 DOI
Siems K., Runzheimer K., Rehm A., Schwengers O., Heidler von Heilborn D., Kaser L., et al. . (2022). Phenotypic and genomic assessment of the potential threat of human spaceflight-relevant Staphylococcus capitis isolates under stress conditions. Front. Microbiol. 13:1007143. doi: 10.3389/fmicb.2022.1007143 PubMed DOI PMC
Siziya I. N., Hwang C. Y., Seo M.-J. (2022). Antioxidant potential and capacity of microorganism-sourced C30 carotenoids—a review. Antioxidants 11:1963. doi: 10.3390/antiox11101963, PMID: PubMed DOI PMC
Sobisch L.-Y., Rogowski K. M., Fuchs J., Schmieder W., Vaishampayan A., Oles P., et al. . (2019). Biofilm forming antibiotic resistant gram-positive pathogens isolated from surfaces on the international Space Station. Front. Microbiol. 10:543. doi: 10.3389/fmicb.2019.00543, PMID: PubMed DOI PMC
Verma S. P., Philippot J. R., Bonnet B., Sainte-Marie J., Moschetto Y., Wallach D. F. (1984). Resonance Raman spectra of beta-carotene in native and modified low-density lipoprotein. Biochem. Biophys. Res. Commun. 122, 867–875. doi: 10.1016/S0006-291X(84)80114-X, PMID: PubMed DOI
ViroxTechnologies (2018). AHP goes beyond. Available at: https://virox.com/making-news/virox-corp-news/ahp-goes-beyond/ (Accessed August 31, 2023).
Watanabe S., Aiba Y., Tan X.-E., Li F.-Y., Boonsiri T., Thitiananpakorn K., et al. . (2018). Complete genome sequencing of three human clinical isolates of Staphylococcus caprae reveals virulence factors similar to those of S. epidermidis and S. capitis. BMC Genomics 19:810. doi: 10.1186/s12864-018-5185-9 PubMed DOI PMC
Wieland B., Feil C., Gloria-Maercker E., Thumm G., Lechner M., Bravo J. M., et al. . (1994). Genetic and biochemical analyses of the biosynthesis of the yellow carotenoid 4,4′-diaponeurosporene of Staphylococcus aureus. J. Bacteriol. 176, 7719–7726. doi: 10.1128/jb.176.24.7719-7726.1994, PMID: PubMed DOI PMC
Wirth T., Bergot M., Rasigade J.-P., Pichon B., Barbier M., Martins-Simoes P., et al. . (2020). Niche specialization and spread of Staphylococcus capitis involved in neonatal sepsis. Nat. Microbiol. 5, 735–745. doi: 10.1038/s41564-020-0676-2, PMID: PubMed DOI
Xue L., Chen Y. Y., Yan Z., Lu W., Wan D., Zhu H. (2019). Staphyloxanthin: a potential target for antivirulence therapy. Infect. Drug Resist. 12:2151. doi: 10.2147/IDR.S193649 PubMed DOI PMC
Yao Z. Y., Qi J. H. (2016). Comparison of antioxidant activities of melanin fractions from chestnut Shell. Molecules 21:487. doi: 10.3390/molecules21040487, PMID: PubMed DOI PMC