Cytokinin Signaling in <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>

ABSTRACT It was recently reported that the human-exclusive pathogen Mycobacterium tuberculosis secretes cytokinins, which had only been known as plant hormones. While cytokinins are well-established, adenine-based signaling molecules in plants, they have never been shown to participate in signal tra...

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Main Authors: Marie I. Samanovic, Hao-Chi Hsu, Marcus B. Jones, Victoria Jones, Michael R. McNeil, Samuel H. Becker, Ashley T. Jordan, Miroslav Strnad, Changcheng Xu, Mary Jackson, Huilin Li, K. Heran Darwin
Format: Article
Language:English
Published: American Society for Microbiology 2018-07-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mBio.00989-18
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author Marie I. Samanovic
Hao-Chi Hsu
Marcus B. Jones
Victoria Jones
Michael R. McNeil
Samuel H. Becker
Ashley T. Jordan
Miroslav Strnad
Changcheng Xu
Mary Jackson
Huilin Li
K. Heran Darwin
author_facet Marie I. Samanovic
Hao-Chi Hsu
Marcus B. Jones
Victoria Jones
Michael R. McNeil
Samuel H. Becker
Ashley T. Jordan
Miroslav Strnad
Changcheng Xu
Mary Jackson
Huilin Li
K. Heran Darwin
author_sort Marie I. Samanovic
collection DOAJ
description ABSTRACT It was recently reported that the human-exclusive pathogen Mycobacterium tuberculosis secretes cytokinins, which had only been known as plant hormones. While cytokinins are well-established, adenine-based signaling molecules in plants, they have never been shown to participate in signal transduction in other kingdoms of life. M. tuberculosis is not known to interact with plants. Therefore, we tested the hypothesis that cytokinins trigger transcriptional changes within this bacterial species. Here, we show cytokinins induced the strong expression of the M. tuberculosis gene Rv0077c. We found that Rv0077c expression is repressed by a TetR-like transcriptional repressor, Rv0078. Strikingly, cytokinin-induced expression of Rv0077c resulted in a loss of acid-fast staining of M. tuberculosis. While acid-fast staining is thought to be associated with changes in the bacterial cell envelope and virulence, Rv0077c-induced loss of acid-fastness did not affect antibiotic susceptibility or attenuate bacterial growth in mice, consistent with an unaltered mycolic acid profile of Rv0077c-expressing cells. Collectively, these findings show cytokinins signal transcriptional changes that can affect M. tuberculosis acid-fastness and that cytokinin signaling is no longer limited to the kingdom Plantae. IMPORTANCE Cytokinins have only previously been known as plant hormones. The discovery that they can be used as signaling molecules outside of plants broadens the repertoire of small molecules that can potentially affect gene expression in all domains of life.
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spelling doaj.art-8cd03f758378472fbebf93b3106723bd2022-12-21T20:47:45ZengAmerican Society for MicrobiologymBio2150-75112018-07-019310.1128/mBio.00989-18Cytokinin Signaling in <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>Marie I. Samanovic0Hao-Chi Hsu1Marcus B. Jones2Victoria Jones3Michael R. McNeil4Samuel H. Becker5Ashley T. Jordan6Miroslav Strnad7Changcheng Xu8Mary Jackson9Huilin Li10K. Heran Darwin11Department of Microbiology, New York University School of Medicine, New York, New York, USAVan Andel Research Institute, Grand Rapids, Michigan, USAHuman Longevity, Inc., San Diego, California, USAMycobacteria Research Laboratories, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USAMycobacteria Research Laboratories, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USADepartment of Microbiology, New York University School of Medicine, New York, New York, USADepartment of Microbiology, New York University School of Medicine, New York, New York, USALaboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany ASCR and Palacký University, Olomouc, Czech RepublicBiology Department, Brookhaven National Laboratory, Upton, New York, USAMycobacteria Research Laboratories, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USAVan Andel Research Institute, Grand Rapids, Michigan, USADepartment of Microbiology, New York University School of Medicine, New York, New York, USAABSTRACT It was recently reported that the human-exclusive pathogen Mycobacterium tuberculosis secretes cytokinins, which had only been known as plant hormones. While cytokinins are well-established, adenine-based signaling molecules in plants, they have never been shown to participate in signal transduction in other kingdoms of life. M. tuberculosis is not known to interact with plants. Therefore, we tested the hypothesis that cytokinins trigger transcriptional changes within this bacterial species. Here, we show cytokinins induced the strong expression of the M. tuberculosis gene Rv0077c. We found that Rv0077c expression is repressed by a TetR-like transcriptional repressor, Rv0078. Strikingly, cytokinin-induced expression of Rv0077c resulted in a loss of acid-fast staining of M. tuberculosis. While acid-fast staining is thought to be associated with changes in the bacterial cell envelope and virulence, Rv0077c-induced loss of acid-fastness did not affect antibiotic susceptibility or attenuate bacterial growth in mice, consistent with an unaltered mycolic acid profile of Rv0077c-expressing cells. Collectively, these findings show cytokinins signal transcriptional changes that can affect M. tuberculosis acid-fastness and that cytokinin signaling is no longer limited to the kingdom Plantae. IMPORTANCE Cytokinins have only previously been known as plant hormones. The discovery that they can be used as signaling molecules outside of plants broadens the repertoire of small molecules that can potentially affect gene expression in all domains of life.https://journals.asm.org/doi/10.1128/mBio.00989-18Mycobacterium tuberculosisacid-fast stainingcytokininregulationsignaling
spellingShingle Marie I. Samanovic
Hao-Chi Hsu
Marcus B. Jones
Victoria Jones
Michael R. McNeil
Samuel H. Becker
Ashley T. Jordan
Miroslav Strnad
Changcheng Xu
Mary Jackson
Huilin Li
K. Heran Darwin
Cytokinin Signaling in <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>
mBio
Mycobacterium tuberculosis
acid-fast staining
cytokinin
regulation
signaling
title Cytokinin Signaling in <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>
title_full Cytokinin Signaling in <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>
title_fullStr Cytokinin Signaling in <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>
title_full_unstemmed Cytokinin Signaling in <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>
title_short Cytokinin Signaling in <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>
title_sort cytokinin signaling in named content content type genus species mycobacterium tuberculosis named content
topic Mycobacterium tuberculosis
acid-fast staining
cytokinin
regulation
signaling
url https://journals.asm.org/doi/10.1128/mBio.00989-18
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