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Epinephrine Affects Ribosomes, Cell Division, and Catabolic Processes in Micrococcus luteus Skin Strain C01: Revelation of the Conditionally Extensive Hormone Effect Using Orbitrap Mass Spectrometry and Proteomic Analysis

SIMPLE SUMMARY: In recent decades, more and more data have been accumulated on the close interaction of the human microbiota with the human organism. Today, we can safely say that human hormones are microbiota regulators that can influence both the behavior of individual species and the balance of m...

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Autores principales: Gannesen, Andrei V., Ziganshin, Rustam H., Ovcharova, Maria A., Nevolina, Ekaterina D., Klimko, Alena I., Martyanov, Sergey V., Plakunov, Vladimir K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10535722/
https://www.ncbi.nlm.nih.gov/pubmed/37764026
http://dx.doi.org/10.3390/microorganisms11092181
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author Gannesen, Andrei V.
Ziganshin, Rustam H.
Ovcharova, Maria A.
Nevolina, Ekaterina D.
Klimko, Alena I.
Martyanov, Sergey V.
Plakunov, Vladimir K.
author_facet Gannesen, Andrei V.
Ziganshin, Rustam H.
Ovcharova, Maria A.
Nevolina, Ekaterina D.
Klimko, Alena I.
Martyanov, Sergey V.
Plakunov, Vladimir K.
author_sort Gannesen, Andrei V.
collection PubMed
description SIMPLE SUMMARY: In recent decades, more and more data have been accumulated on the close interaction of the human microbiota with the human organism. Today, we can safely say that human hormones are microbiota regulators that can influence both the behavior of individual species and the balance of microbial communities. However, the mechanisms of such action have been elucidated for an extremely small number of microorganisms. In particular, very little is known about how hormones, especially catecholamines, affect skin Gram-positive microorganisms and their biofilms. In our work, we studied for the first time how epinephrine at a concentration close to normal in blood plasma affects the protein composition of planktonic cultures and biofilms of the skin microorganism Micrococcus luteus C01, as well as how the protein composition changes depending on the cultivation time. It was shown that despite the small number of genes with altered expression in the presence of the hormone, the concentration of dozens and hundreds of proteins changes in the presence of epinephrine. The main “targets” of epinephrine are proteins of ribosomes, the tricarboxylic acid cycle, and cell division. Thus, this study opens up great prospects for further work in the field of microbial endocrinology. ABSTRACT: In the current study, extensive Orbitrap mass spectrometry analysis was conducted for skin strain Micrococcus luteus C01 planktonic cultures and biofilms after 24 h and 72 h of incubation either in the presence of epinephrine or without any implementations. The investigation revealed the complex and conditionally extensive effect of epinephrine at concentrations closer to normal blood plasma concentrations on both planktonic cultures and biofilms of skin strain M. luteus C01. The concentrations of hundreds of proteins changed during the shift from planktonic growth mode to biofilm and hundreds of proteins were downregulated or upregulated in the presence of epinephrine. Ribosomal, TCA, and cell division proteins appear to be the most altered in their amounts in the presence of the hormone. Potentially, the regulatory mechanism of this process is connected with c-di-GMP and histidine kinases, which were affected by epinephrine in different samples. The phenomenon of epinephrine-based biofilm regulation in M. luteus C01 has wide implications for microbial endocrinology and other research areas.
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spelling pubmed-105357222023-09-29 Epinephrine Affects Ribosomes, Cell Division, and Catabolic Processes in Micrococcus luteus Skin Strain C01: Revelation of the Conditionally Extensive Hormone Effect Using Orbitrap Mass Spectrometry and Proteomic Analysis Gannesen, Andrei V. Ziganshin, Rustam H. Ovcharova, Maria A. Nevolina, Ekaterina D. Klimko, Alena I. Martyanov, Sergey V. Plakunov, Vladimir K. Microorganisms Article SIMPLE SUMMARY: In recent decades, more and more data have been accumulated on the close interaction of the human microbiota with the human organism. Today, we can safely say that human hormones are microbiota regulators that can influence both the behavior of individual species and the balance of microbial communities. However, the mechanisms of such action have been elucidated for an extremely small number of microorganisms. In particular, very little is known about how hormones, especially catecholamines, affect skin Gram-positive microorganisms and their biofilms. In our work, we studied for the first time how epinephrine at a concentration close to normal in blood plasma affects the protein composition of planktonic cultures and biofilms of the skin microorganism Micrococcus luteus C01, as well as how the protein composition changes depending on the cultivation time. It was shown that despite the small number of genes with altered expression in the presence of the hormone, the concentration of dozens and hundreds of proteins changes in the presence of epinephrine. The main “targets” of epinephrine are proteins of ribosomes, the tricarboxylic acid cycle, and cell division. Thus, this study opens up great prospects for further work in the field of microbial endocrinology. ABSTRACT: In the current study, extensive Orbitrap mass spectrometry analysis was conducted for skin strain Micrococcus luteus C01 planktonic cultures and biofilms after 24 h and 72 h of incubation either in the presence of epinephrine or without any implementations. The investigation revealed the complex and conditionally extensive effect of epinephrine at concentrations closer to normal blood plasma concentrations on both planktonic cultures and biofilms of skin strain M. luteus C01. The concentrations of hundreds of proteins changed during the shift from planktonic growth mode to biofilm and hundreds of proteins were downregulated or upregulated in the presence of epinephrine. Ribosomal, TCA, and cell division proteins appear to be the most altered in their amounts in the presence of the hormone. Potentially, the regulatory mechanism of this process is connected with c-di-GMP and histidine kinases, which were affected by epinephrine in different samples. The phenomenon of epinephrine-based biofilm regulation in M. luteus C01 has wide implications for microbial endocrinology and other research areas. MDPI 2023-08-29 /pmc/articles/PMC10535722/ /pubmed/37764026 http://dx.doi.org/10.3390/microorganisms11092181 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
Gannesen, Andrei V.
Ziganshin, Rustam H.
Ovcharova, Maria A.
Nevolina, Ekaterina D.
Klimko, Alena I.
Martyanov, Sergey V.
Plakunov, Vladimir K.
Epinephrine Affects Ribosomes, Cell Division, and Catabolic Processes in Micrococcus luteus Skin Strain C01: Revelation of the Conditionally Extensive Hormone Effect Using Orbitrap Mass Spectrometry and Proteomic Analysis
title Epinephrine Affects Ribosomes, Cell Division, and Catabolic Processes in Micrococcus luteus Skin Strain C01: Revelation of the Conditionally Extensive Hormone Effect Using Orbitrap Mass Spectrometry and Proteomic Analysis
title_full Epinephrine Affects Ribosomes, Cell Division, and Catabolic Processes in Micrococcus luteus Skin Strain C01: Revelation of the Conditionally Extensive Hormone Effect Using Orbitrap Mass Spectrometry and Proteomic Analysis
title_fullStr Epinephrine Affects Ribosomes, Cell Division, and Catabolic Processes in Micrococcus luteus Skin Strain C01: Revelation of the Conditionally Extensive Hormone Effect Using Orbitrap Mass Spectrometry and Proteomic Analysis
title_full_unstemmed Epinephrine Affects Ribosomes, Cell Division, and Catabolic Processes in Micrococcus luteus Skin Strain C01: Revelation of the Conditionally Extensive Hormone Effect Using Orbitrap Mass Spectrometry and Proteomic Analysis
title_short Epinephrine Affects Ribosomes, Cell Division, and Catabolic Processes in Micrococcus luteus Skin Strain C01: Revelation of the Conditionally Extensive Hormone Effect Using Orbitrap Mass Spectrometry and Proteomic Analysis
title_sort epinephrine affects ribosomes, cell division, and catabolic processes in micrococcus luteus skin strain c01: revelation of the conditionally extensive hormone effect using orbitrap mass spectrometry and proteomic analysis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10535722/
https://www.ncbi.nlm.nih.gov/pubmed/37764026
http://dx.doi.org/10.3390/microorganisms11092181
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