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Article

Inhibition of Biofilm Formation in Cutibacterium acnes, Staphylococcus aureus, and Candida albicans by the Phytopigment Shikonin

by
Yong-Guy Kim
1,†,
Jin-Hyung Lee
1,†,
Sanghun Kim
1,
Sunyoung Park
1,
Yu-Jeong Kim
2,
Choong-Min Ryu
2,3,
Hwi Won Seo
3,* and
Jintae Lee
1,*
1
School of Chemical Engineering, Yeungnam University, 280 Daehak-Ro, Gyeongsan 38541, Republic of Korea
2
Biosystems & Bioengineering Program, University of Science and Technology (UST), Daejeon Campus, Daejeon 34113, Republic of Korea
3
Infectious Disease Research Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon 34141, Republic of Korea
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2024, 25(4), 2426; https://doi.org/10.3390/ijms25042426
Submission received: 26 January 2024 / Revised: 14 February 2024 / Accepted: 15 February 2024 / Published: 19 February 2024
(This article belongs to the Special Issue New Insights in Bioactive Compounds as Antibiofilm Agents)
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Abstract

Skin microbiota, such as acne-related Cutibacterium acnes, Staphylococcus aureus, and fungal Candida albicans, can form polymicrobial biofilms with greater antimicrobial tolerance to traditional antimicrobial agents and host immune systems. In this study, the phytopigment shikonin was investigated against single-species and multispecies biofilms under aerobic and anaerobic conditions. Minimum inhibitory concentrations of shikonin were 10 µg/mL against C. acnes, S. aureus, and C. albicans, and at 1–5 µg/mL, shikonin efficiently inhibited single biofilm formation and multispecies biofilm development by these three microbes. Shikonin increased porphyrin production in C. acnes, inhibited cell aggregation and hyphal formation by C. albicans, decreased lipase production, and increased hydrophilicity in S. aureus. In addition, shikonin at 5 or 10 µg/mL repressed the transcription of various biofilm-related genes and virulence-related genes in C. acnes and downregulated the gene expression levels of the quorum-sensing agrA and RNAIII, α-hemolysin hla, and nuclease nuc1 in S. aureus, supporting biofilm inhibition. In addition, shikonin prevented multispecies biofilm development on porcine skin, and the antimicrobial efficacy of shikonin was recapitulated in a mouse infection model, in which it promoted skin regeneration. The study shows that shikonin inhibits multispecies biofilm development by acne-related skin microbes and might be useful for controlling bacterial infections.
Keywords: Candida albicans; Cutibacterium acnes; polymicrobial biofilms; shikonin; Staphylococcus aureus Candida albicans; Cutibacterium acnes; polymicrobial biofilms; shikonin; Staphylococcus aureus

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MDPI and ACS Style

Kim, Y.-G.; Lee, J.-H.; Kim, S.; Park, S.; Kim, Y.-J.; Ryu, C.-M.; Seo, H.W.; Lee, J. Inhibition of Biofilm Formation in Cutibacterium acnes, Staphylococcus aureus, and Candida albicans by the Phytopigment Shikonin. Int. J. Mol. Sci. 2024, 25, 2426. https://doi.org/10.3390/ijms25042426

AMA Style

Kim Y-G, Lee J-H, Kim S, Park S, Kim Y-J, Ryu C-M, Seo HW, Lee J. Inhibition of Biofilm Formation in Cutibacterium acnes, Staphylococcus aureus, and Candida albicans by the Phytopigment Shikonin. International Journal of Molecular Sciences. 2024; 25(4):2426. https://doi.org/10.3390/ijms25042426

Chicago/Turabian Style

Kim, Yong-Guy, Jin-Hyung Lee, Sanghun Kim, Sunyoung Park, Yu-Jeong Kim, Choong-Min Ryu, Hwi Won Seo, and Jintae Lee. 2024. "Inhibition of Biofilm Formation in Cutibacterium acnes, Staphylococcus aureus, and Candida albicans by the Phytopigment Shikonin" International Journal of Molecular Sciences 25, no. 4: 2426. https://doi.org/10.3390/ijms25042426

APA Style

Kim, Y.-G., Lee, J.-H., Kim, S., Park, S., Kim, Y.-J., Ryu, C.-M., Seo, H. W., & Lee, J. (2024). Inhibition of Biofilm Formation in Cutibacterium acnes, Staphylococcus aureus, and Candida albicans by the Phytopigment Shikonin. International Journal of Molecular Sciences, 25(4), 2426. https://doi.org/10.3390/ijms25042426

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