Proteomic and transcriptomic analyses of <i>Cutibacterium acnes</i> biofilms and planktonic cultures in presence of epinephrine

AV Gannesen; MI Schelkunov; RH Ziganshin; MA Ovcharova; MV Sukhacheva; NE Makarova; SV Mart'yanov; NA Loginova; AM Mosolova; EV Diuvenji; ED Nevolina; VK Plakunov; AV Gannesen; MI Schelkunov; RH Ziganshin; MA Ovcharova; MV Sukhacheva; NE Makarova; SV Mart'yanov; NA Loginova; AM Mosolova; EV Diuvenji; ED Nevolina; VK Plakunov

doi:10.3934/microbiol.2024019

AIMS Microbiology

2024, Volume 10, Issue 2: 363-390. doi: 10.3934/microbiol.2024019

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Proteomic and transcriptomic analyses of Cutibacterium acnes biofilms and planktonic cultures in presence of epinephrine

1.
Federal Research Centre “Fundamentals of Biotechnology” of Russian Academy of Sciences, Moscow 119071, Russia
2.
Skolkovo Institute of Science and Technology, Moscow 121205, Russia
3.
Institute for Information Transmission Problems of Russian Academy of Sciences, Moscow 127051, Russia
4.
Institute of Bioorganic Chemistry, Russian Academy of Sciences, Moscow 117997, Russia
5.
Russian Biotechnological University, Moscow 125080, Russia

Received: 04 March 2024 Revised: 15 May 2024 Accepted: 21 May 2024 Published: 27 May 2024

Transcriptomic and proteomic analysis were performed on 72 h biofilms of the acneic strain Cutibacterium acnes and planktonic cultures in the presence of epinephrine. Epinephrine predominantly downregulated genes associated with various transporter proteins. No correlation was found between proteomic and transcriptomic profiles. In control samples, the expression of 51 proteins differed between planktonic cultures and biofilms. Addition of 5 nM epinephrine reduced this number, and in the presence of 5 µM epinephrine, the difference in proteomic profiles between planktonic cultures and biofilms disappeared. According to the proteomic profiling, epinephrine itself was more effective in the case of C. acnes biofilms and potentially affected the tricarboxylic acid cycle (as well as alpha-ketoglutarate decarboxylase Kgd), biotin synthesis, cell division, and transport of different compounds in C. acnes cells. These findings are consistent with recent research on Micrococcus luteus, suggesting that the effects of epinephrine on actinobacteria may be universal.
- biofilms,
- Cutibacterium acnes,
- microbial endocrinology,
- proteomics,
- transcriptomics,
- RNA-Seq,
- qRT-PCR,
- epinephrine,
- hormones,
- skin microbiota
Citation: AV Gannesen, MI Schelkunov, RH Ziganshin, MA Ovcharova, MV Sukhacheva, NE Makarova, SV Mart'yanov, NA Loginova, AM Mosolova, EV Diuvenji, ED Nevolina, VK Plakunov. Proteomic and transcriptomic analyses of Cutibacterium acnes biofilms and planktonic cultures in presence of epinephrine[J]. AIMS Microbiology, 2024, 10(2): 363-390. doi: 10.3934/microbiol.2024019

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Abstract

Transcriptomic and proteomic analysis were performed on 72 h biofilms of the acneic strain Cutibacterium acnes and planktonic cultures in the presence of epinephrine. Epinephrine predominantly downregulated genes associated with various transporter proteins. No correlation was found between proteomic and transcriptomic profiles. In control samples, the expression of 51 proteins differed between planktonic cultures and biofilms. Addition of 5 nM epinephrine reduced this number, and in the presence of 5 µM epinephrine, the difference in proteomic profiles between planktonic cultures and biofilms disappeared. According to the proteomic profiling, epinephrine itself was more effective in the case of C. acnes biofilms and potentially affected the tricarboxylic acid cycle (as well as alpha-ketoglutarate decarboxylase Kgd), biotin synthesis, cell division, and transport of different compounds in C. acnes cells. These findings are consistent with recent research on Micrococcus luteus, suggesting that the effects of epinephrine on actinobacteria may be universal.

Acknowledgments

Transcriptome sequencing and analysis were performed in the Genomics Core Facility of the Skolkovo Institute of Science and Technology (https://www.skoltech.ru/research/en/gcf-2/ (accessed on March1, 2024). qRT–PCR was performed using the scientific equipment of the Core Research Facility ‘Bioengineering’ (Research Center of Biotechnology RAS). A.V. Gannesen and coauthors sincerely thank V.V. Sorokin and A.V. Mulyukin (Core Facility “UNIQEM collection” of Research Center of Biotechnology RAS) for their kind assistance and for providing liquid nitrogen for this study. The authors are grateful to the staff of the Laboratory of Molecular Ecology and Phylogenomics of Bacteria of the Research Center of Biotechnology RAS (the head Svetlana N. Dedysh) and, personally to Svetlana E. Belova, Igor. Yu. Oshkin, Kirill K. Miroshnikov, and Anastasiya A. Ivanova for their kind assistance and giving access to the FastPrep disintegrator. Authors cordially thank Maya M. Polovitskaya for her kind assistance in the editing of the manuscript.

Funding

The work is supported by the RSCF, the grant nº 19-74-10071. The work of V.K. Plakunov is supported by the Ministry of Science and Higher Education of Russian Federation.

Conflict of interests

Authors declare no conflict of interests.

Data availability statement

The transcriptomic data are deposited at the Sequence Read Archive (SRA) database under the identifiers SRR27884912 and SRR27884920. The mass spectrometry proteomics data have been deposited at the ProteomeXchange Consortium via the PRIDE partner repository [57]–[58] with the data set identifier PXD049410.

Author contributions

Conceptualization, A.V.G.; investigation, M.A.O., M.I.S., R.H.Z., N.A.L., A.M.M., N.E.M., S.V.M., E.D.N., E.D.V. and A.V.G.; validation, M.A.O., M.I.S., S.V.M., R.H.Z., N.A.L., A.M.M., N.E.M., S.V.M., E.D.N., V.K.P., and A.V.G.; formal analysis, M.A.O., M.I.S., R.H.Z., and A.V.G.; writing—original draft, M.A.O., M.I.S., S.V.M., R.H.Z., E.D.N., N.E.M., N.A.L., A.M.M., E.D.V., and A.V.G.; data curation, M.A.O., M.I.S., R.H.Z., N.E.M., and A.V.G.; writing—review and editing, M.A.O., M.I.S., R.H.Z., S.V.M., V.K.P. and A.V.G.; visualization, M.A.O., M.I.S., R.H.Z., S.V.M., E.D.N., N.A.L., A.M.M., and A.V.G.; supervision, V.K.P. and A.V.G.; resources, A.V.G.; funding acquisition, A.V.G.; project administration, A.V.G. All authors have read and agreed to the published version of the manuscript.

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