Heterologous Production of 1-Tuberculosinyladenosine in <named-content content-type="genus-species">Mycobacterium kansasii</named-content> Models Pathoevolution towards the Transcellular Lifestyle of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>

ABSTRACT Mycobacterium kansasii is an environmental nontuberculous mycobacterium that causes opportunistic tuberculosis-like disease. It is one of the most closely related species to the Mycobacterium tuberculosis complex. Using M. kansasii as a proxy for the M. kansasii-M. tuberculosis common ances...

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Autores principales:	Marwan Ghanem, Jean-Yves Dubé, Joyce Wang, Fiona McIntosh, Daniel Houle, Pilar Domenech, Michael B. Reed, Sahadevan Raman, Jeffrey Buter, Adriaan J. Minnaard, D. Branch Moody, Marcel A. Behr
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	1-TbAd Mycobacterium kansasii Mycobacterium tuberculosis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8ba23b5acfc14efd85b332b2f35beb17
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spelling	oai:doaj.org-article:8ba23b5acfc14efd85b332b2f35beb172021-11-15T16:19:08ZHeterologous Production of 1-Tuberculosinyladenosine in <named-content content-type="genus-species">Mycobacterium kansasii</named-content> Models Pathoevolution towards the Transcellular Lifestyle of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>10.1128/mBio.02645-202150-7511https://doaj.org/article/8ba23b5acfc14efd85b332b2f35beb172020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02645-20https://doaj.org/toc/2150-7511ABSTRACT Mycobacterium kansasii is an environmental nontuberculous mycobacterium that causes opportunistic tuberculosis-like disease. It is one of the most closely related species to the Mycobacterium tuberculosis complex. Using M. kansasii as a proxy for the M. kansasii-M. tuberculosis common ancestor, we asked whether introducing the M. tuberculosis-specific gene pair Rv3377c-Rv3378c into M. kansasii affects the course of experimental infection. Expression of these genes resulted in the production of an adenosine-linked lipid species, known as 1-tuberculosinyladenosine (1-TbAd), but did not alter growth in vitro under standard conditions. Production of 1-TbAd enhanced growth of M. kansasii under acidic conditions through a bacterial cell-intrinsic mechanism independent of controlling pH in the bulk extracellular and intracellular spaces. Production of 1-TbAd led to greater burden of M. kansasii in the lungs of C57BL/6 mice during the first 24 h after infection, and ex vivo infections of alveolar macrophages recapitulated this phenotype within the same time frame. However, in long-term infections, production of 1-TbAd resulted in impaired bacterial survival in both C57BL/6 mice and Ccr2−/− mice. We have demonstrated that M. kansasii is a valid surrogate of M. tuberculosis to study virulence factors acquired by the latter organism, yet shown the challenge inherent to studying the complex evolution of mycobacterial pathogenicity with isolated gene complementation. IMPORTANCE This work sheds light on the role of the lipid 1-tuberculosinyladenosine in the evolution of an environmental ancestor to M. tuberculosis. On a larger scale, it reinforces the importance of horizontal gene transfer in bacterial evolution and examines novel models and methods to provide a better understanding of the subtle effects of individual M. tuberculosis-specific virulence factors in infection settings that are relevant to the pathogen.Marwan GhanemJean-Yves DubéJoyce WangFiona McIntoshDaniel HoulePilar DomenechMichael B. ReedSahadevan RamanJeffrey ButerAdriaan J. MinnaardD. Branch MoodyMarcel A. BehrAmerican Society for Microbiologyarticle1-TbAdMycobacterium kansasiiMycobacterium tuberculosisMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	1-TbAd Mycobacterium kansasii Mycobacterium tuberculosis Microbiology QR1-502
spellingShingle	1-TbAd Mycobacterium kansasii Mycobacterium tuberculosis Microbiology QR1-502 Marwan Ghanem Jean-Yves Dubé Joyce Wang Fiona McIntosh Daniel Houle Pilar Domenech Michael B. Reed Sahadevan Raman Jeffrey Buter Adriaan J. Minnaard D. Branch Moody Marcel A. Behr Heterologous Production of 1-Tuberculosinyladenosine in <named-content content-type="genus-species">Mycobacterium kansasii</named-content> Models Pathoevolution towards the Transcellular Lifestyle of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>
description	ABSTRACT Mycobacterium kansasii is an environmental nontuberculous mycobacterium that causes opportunistic tuberculosis-like disease. It is one of the most closely related species to the Mycobacterium tuberculosis complex. Using M. kansasii as a proxy for the M. kansasii-M. tuberculosis common ancestor, we asked whether introducing the M. tuberculosis-specific gene pair Rv3377c-Rv3378c into M. kansasii affects the course of experimental infection. Expression of these genes resulted in the production of an adenosine-linked lipid species, known as 1-tuberculosinyladenosine (1-TbAd), but did not alter growth in vitro under standard conditions. Production of 1-TbAd enhanced growth of M. kansasii under acidic conditions through a bacterial cell-intrinsic mechanism independent of controlling pH in the bulk extracellular and intracellular spaces. Production of 1-TbAd led to greater burden of M. kansasii in the lungs of C57BL/6 mice during the first 24 h after infection, and ex vivo infections of alveolar macrophages recapitulated this phenotype within the same time frame. However, in long-term infections, production of 1-TbAd resulted in impaired bacterial survival in both C57BL/6 mice and Ccr2−/− mice. We have demonstrated that M. kansasii is a valid surrogate of M. tuberculosis to study virulence factors acquired by the latter organism, yet shown the challenge inherent to studying the complex evolution of mycobacterial pathogenicity with isolated gene complementation. IMPORTANCE This work sheds light on the role of the lipid 1-tuberculosinyladenosine in the evolution of an environmental ancestor to M. tuberculosis. On a larger scale, it reinforces the importance of horizontal gene transfer in bacterial evolution and examines novel models and methods to provide a better understanding of the subtle effects of individual M. tuberculosis-specific virulence factors in infection settings that are relevant to the pathogen.
format	article
author	Marwan Ghanem Jean-Yves Dubé Joyce Wang Fiona McIntosh Daniel Houle Pilar Domenech Michael B. Reed Sahadevan Raman Jeffrey Buter Adriaan J. Minnaard D. Branch Moody Marcel A. Behr
author_facet	Marwan Ghanem Jean-Yves Dubé Joyce Wang Fiona McIntosh Daniel Houle Pilar Domenech Michael B. Reed Sahadevan Raman Jeffrey Buter Adriaan J. Minnaard D. Branch Moody Marcel A. Behr
author_sort	Marwan Ghanem
title	Heterologous Production of 1-Tuberculosinyladenosine in <named-content content-type="genus-species">Mycobacterium kansasii</named-content> Models Pathoevolution towards the Transcellular Lifestyle of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>
title_short	Heterologous Production of 1-Tuberculosinyladenosine in <named-content content-type="genus-species">Mycobacterium kansasii</named-content> Models Pathoevolution towards the Transcellular Lifestyle of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>
title_full	Heterologous Production of 1-Tuberculosinyladenosine in <named-content content-type="genus-species">Mycobacterium kansasii</named-content> Models Pathoevolution towards the Transcellular Lifestyle of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>
title_fullStr	Heterologous Production of 1-Tuberculosinyladenosine in <named-content content-type="genus-species">Mycobacterium kansasii</named-content> Models Pathoevolution towards the Transcellular Lifestyle of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>
title_full_unstemmed	Heterologous Production of 1-Tuberculosinyladenosine in <named-content content-type="genus-species">Mycobacterium kansasii</named-content> Models Pathoevolution towards the Transcellular Lifestyle of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>
title_sort	heterologous production of 1-tuberculosinyladenosine in <named-content content-type="genus-species">mycobacterium kansasii</named-content> models pathoevolution towards the transcellular lifestyle of <named-content content-type="genus-species">mycobacterium tuberculosis</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/8ba23b5acfc14efd85b332b2f35beb17
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Heterologous Production of 1-Tuberculosinyladenosine in <named-content content-type="genus-species">Mycobacterium kansasii</named-content> Models Pathoevolution towards the Transcellular Lifestyle of <named-content content-type="genus-species">Mycobacterium tuberculosis</named-content>

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