The Ribbon-Helix-Helix Domain Protein CdrS Regulates the Tubulin Homolog <italic toggle="yes">ftsZ2</italic> To Control Cell Division in Archaea

ABSTRACT Precise control of the cell cycle is central to the physiology of all cells. In prior work we demonstrated that archaeal cells maintain a constant size; however, the regulatory mechanisms underlying the cell cycle remain unexplored in this domain of life. Here, we use genetics, functional g...

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Autores principales: Cynthia L. Darnell, Jenny Zheng, Sean Wilson, Ryan M. Bertoli, Alexandre W. Bisson-Filho, Ethan C. Garner, Amy K. Schmid
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:efe91ec2cd5b4204ab3646133fe6130f2021-11-15T15:56:43ZThe Ribbon-Helix-Helix Domain Protein CdrS Regulates the Tubulin Homolog <italic toggle="yes">ftsZ2</italic> To Control Cell Division in Archaea10.1128/mBio.01007-202150-7511https://doaj.org/article/efe91ec2cd5b4204ab3646133fe6130f2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01007-20https://doaj.org/toc/2150-7511ABSTRACT Precise control of the cell cycle is central to the physiology of all cells. In prior work we demonstrated that archaeal cells maintain a constant size; however, the regulatory mechanisms underlying the cell cycle remain unexplored in this domain of life. Here, we use genetics, functional genomics, and quantitative imaging to identify and characterize the novel CdrSL gene regulatory network in a model species of archaea. We demonstrate the central role of these ribbon-helix-helix family transcription factors in the regulation of cell division through specific transcriptional control of the gene encoding FtsZ2, a putative tubulin homolog. Using time-lapse fluorescence microscopy in live cells cultivated in microfluidics devices, we further demonstrate that FtsZ2 is required for cell division but not elongation. The cdrS-ftsZ2 locus is highly conserved throughout the archaeal domain, and the central function of CdrS in regulating cell division is conserved across hypersaline adapted archaea. We propose that the CdrSL-FtsZ2 transcriptional network coordinates cell division timing with cell growth in archaea. IMPORTANCE Healthy cell growth and division are critical for individual organism survival and species long-term viability. However, it remains unknown how cells of the domain Archaea maintain a healthy cell cycle. Understanding the archaeal cell cycle is of paramount evolutionary importance given that an archaeal cell was the host of the endosymbiotic event that gave rise to eukaryotes. Here, we identify and characterize novel molecular players needed for regulating cell division in archaea. These molecules dictate the timing of cell septation but are dispensable for growth between divisions. Timing is accomplished through transcriptional control of the cell division ring. Our results shed light on mechanisms underlying the archaeal cell cycle, which has thus far remained elusive.Cynthia L. DarnellJenny ZhengSean WilsonRyan M. BertoliAlexandre W. Bisson-FilhoEthan C. GarnerAmy K. SchmidAmerican Society for Microbiologyarticlearchaeacell divisiongene regulationtranscription factorsvideo microscopyMicrobiologyQR1-502ENmBio, Vol 11, Iss 4 (2020)
institution DOAJ
collection DOAJ
language EN
topic archaea
cell division
gene regulation
transcription factors
video microscopy
Microbiology
QR1-502
spellingShingle archaea
cell division
gene regulation
transcription factors
video microscopy
Microbiology
QR1-502
Cynthia L. Darnell
Jenny Zheng
Sean Wilson
Ryan M. Bertoli
Alexandre W. Bisson-Filho
Ethan C. Garner
Amy K. Schmid
The Ribbon-Helix-Helix Domain Protein CdrS Regulates the Tubulin Homolog <italic toggle="yes">ftsZ2</italic> To Control Cell Division in Archaea
description ABSTRACT Precise control of the cell cycle is central to the physiology of all cells. In prior work we demonstrated that archaeal cells maintain a constant size; however, the regulatory mechanisms underlying the cell cycle remain unexplored in this domain of life. Here, we use genetics, functional genomics, and quantitative imaging to identify and characterize the novel CdrSL gene regulatory network in a model species of archaea. We demonstrate the central role of these ribbon-helix-helix family transcription factors in the regulation of cell division through specific transcriptional control of the gene encoding FtsZ2, a putative tubulin homolog. Using time-lapse fluorescence microscopy in live cells cultivated in microfluidics devices, we further demonstrate that FtsZ2 is required for cell division but not elongation. The cdrS-ftsZ2 locus is highly conserved throughout the archaeal domain, and the central function of CdrS in regulating cell division is conserved across hypersaline adapted archaea. We propose that the CdrSL-FtsZ2 transcriptional network coordinates cell division timing with cell growth in archaea. IMPORTANCE Healthy cell growth and division are critical for individual organism survival and species long-term viability. However, it remains unknown how cells of the domain Archaea maintain a healthy cell cycle. Understanding the archaeal cell cycle is of paramount evolutionary importance given that an archaeal cell was the host of the endosymbiotic event that gave rise to eukaryotes. Here, we identify and characterize novel molecular players needed for regulating cell division in archaea. These molecules dictate the timing of cell septation but are dispensable for growth between divisions. Timing is accomplished through transcriptional control of the cell division ring. Our results shed light on mechanisms underlying the archaeal cell cycle, which has thus far remained elusive.
format article
author Cynthia L. Darnell
Jenny Zheng
Sean Wilson
Ryan M. Bertoli
Alexandre W. Bisson-Filho
Ethan C. Garner
Amy K. Schmid
author_facet Cynthia L. Darnell
Jenny Zheng
Sean Wilson
Ryan M. Bertoli
Alexandre W. Bisson-Filho
Ethan C. Garner
Amy K. Schmid
author_sort Cynthia L. Darnell
title The Ribbon-Helix-Helix Domain Protein CdrS Regulates the Tubulin Homolog <italic toggle="yes">ftsZ2</italic> To Control Cell Division in Archaea
title_short The Ribbon-Helix-Helix Domain Protein CdrS Regulates the Tubulin Homolog <italic toggle="yes">ftsZ2</italic> To Control Cell Division in Archaea
title_full The Ribbon-Helix-Helix Domain Protein CdrS Regulates the Tubulin Homolog <italic toggle="yes">ftsZ2</italic> To Control Cell Division in Archaea
title_fullStr The Ribbon-Helix-Helix Domain Protein CdrS Regulates the Tubulin Homolog <italic toggle="yes">ftsZ2</italic> To Control Cell Division in Archaea
title_full_unstemmed The Ribbon-Helix-Helix Domain Protein CdrS Regulates the Tubulin Homolog <italic toggle="yes">ftsZ2</italic> To Control Cell Division in Archaea
title_sort ribbon-helix-helix domain protein cdrs regulates the tubulin homolog <italic toggle="yes">ftsz2</italic> to control cell division in archaea
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/efe91ec2cd5b4204ab3646133fe6130f
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