CdrS Is a Global Transcriptional Regulator Influencing Cell Division in <named-content content-type="genus-species">Haloferax volcanii</named-content>
ABSTRACT Transcriptional regulators that integrate cellular and environmental signals to control cell division are well known in bacteria and eukaryotes, but their existence is poorly understood in archaea. We identified a conserved gene (cdrS) that encodes a small protein and is highly transcribed...
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American Society for Microbiology
2021
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oai:doaj.org-article:345d5fd461e344c58138b48125185e8b2021-11-10T18:37:51ZCdrS Is a Global Transcriptional Regulator Influencing Cell Division in <named-content content-type="genus-species">Haloferax volcanii</named-content>10.1128/mBio.01416-212150-7511https://doaj.org/article/345d5fd461e344c58138b48125185e8b2021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01416-21https://doaj.org/toc/2150-7511ABSTRACT Transcriptional regulators that integrate cellular and environmental signals to control cell division are well known in bacteria and eukaryotes, but their existence is poorly understood in archaea. We identified a conserved gene (cdrS) that encodes a small protein and is highly transcribed in the model archaeon Haloferax volcanii. The cdrS gene could not be deleted, but CRISPR interference (CRISPRi)-mediated repression of the cdrS gene caused slow growth and cell division defects and changed the expression of multiple genes and their products associated with cell division, protein degradation, and metabolism. Consistent with this complex regulatory network, overexpression of cdrS inhibited cell division, whereas overexpression of the operon encoding both CdrS and a tubulin-like cell division protein (FtsZ2) stimulated division. Chromatin immunoprecipitation-DNA sequencing (ChIP-Seq) identified 18 DNA-binding sites of the CdrS protein, including one upstream of the promoter for a cell division gene, ftsZ1, and another upstream of the essential gene dacZ, encoding diadenylate cyclase involved in c-di-AMP signaling, which is implicated in the regulation of cell division. These findings suggest that CdrS is a transcription factor that plays a central role in a regulatory network coordinating metabolism and cell division. IMPORTANCE Cell division is a central mechanism of life and is essential for growth and development. Members of the Bacteria and Eukarya have different mechanisms for cell division, which have been studied in detail. In contrast, cell division in members of the Archaea is still understudied, and its regulation is poorly understood. Interestingly, different cell division machineries appear in members of the Archaea, with the Euryarchaeota using a cell division apparatus based on the tubulin-like cytoskeletal protein FtsZ, as in bacteria. Here, we identify the small protein CdrS as essential for survival and a central regulator of cell division in the euryarchaeon Haloferax volcanii. CdrS also appears to coordinate other cellular pathways, including synthesis of signaling molecules and protein degradation. Our results show that CdrS plays a sophisticated role in cell division, including regulation of numerous associated genes. These findings are expected to initiate investigations into conditional regulation of division in archaea.Yan LiaoVerena VogelSabine HauberJürgen BartelOmer S. AlkhnbashiSandra MaaßThandi S. SchwarzRolf BackofenDörte BecherIain G. DugginAnita MarchfelderAmerican Society for MicrobiologyarticleArchaeaHaloferax volcaniicell divisionsmall proteintranscriptional regulationMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021) |
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Archaea Haloferax volcanii cell division small protein transcriptional regulation Microbiology QR1-502 |
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Archaea Haloferax volcanii cell division small protein transcriptional regulation Microbiology QR1-502 Yan Liao Verena Vogel Sabine Hauber Jürgen Bartel Omer S. Alkhnbashi Sandra Maaß Thandi S. Schwarz Rolf Backofen Dörte Becher Iain G. Duggin Anita Marchfelder CdrS Is a Global Transcriptional Regulator Influencing Cell Division in <named-content content-type="genus-species">Haloferax volcanii</named-content> |
description |
ABSTRACT Transcriptional regulators that integrate cellular and environmental signals to control cell division are well known in bacteria and eukaryotes, but their existence is poorly understood in archaea. We identified a conserved gene (cdrS) that encodes a small protein and is highly transcribed in the model archaeon Haloferax volcanii. The cdrS gene could not be deleted, but CRISPR interference (CRISPRi)-mediated repression of the cdrS gene caused slow growth and cell division defects and changed the expression of multiple genes and their products associated with cell division, protein degradation, and metabolism. Consistent with this complex regulatory network, overexpression of cdrS inhibited cell division, whereas overexpression of the operon encoding both CdrS and a tubulin-like cell division protein (FtsZ2) stimulated division. Chromatin immunoprecipitation-DNA sequencing (ChIP-Seq) identified 18 DNA-binding sites of the CdrS protein, including one upstream of the promoter for a cell division gene, ftsZ1, and another upstream of the essential gene dacZ, encoding diadenylate cyclase involved in c-di-AMP signaling, which is implicated in the regulation of cell division. These findings suggest that CdrS is a transcription factor that plays a central role in a regulatory network coordinating metabolism and cell division. IMPORTANCE Cell division is a central mechanism of life and is essential for growth and development. Members of the Bacteria and Eukarya have different mechanisms for cell division, which have been studied in detail. In contrast, cell division in members of the Archaea is still understudied, and its regulation is poorly understood. Interestingly, different cell division machineries appear in members of the Archaea, with the Euryarchaeota using a cell division apparatus based on the tubulin-like cytoskeletal protein FtsZ, as in bacteria. Here, we identify the small protein CdrS as essential for survival and a central regulator of cell division in the euryarchaeon Haloferax volcanii. CdrS also appears to coordinate other cellular pathways, including synthesis of signaling molecules and protein degradation. Our results show that CdrS plays a sophisticated role in cell division, including regulation of numerous associated genes. These findings are expected to initiate investigations into conditional regulation of division in archaea. |
format |
article |
author |
Yan Liao Verena Vogel Sabine Hauber Jürgen Bartel Omer S. Alkhnbashi Sandra Maaß Thandi S. Schwarz Rolf Backofen Dörte Becher Iain G. Duggin Anita Marchfelder |
author_facet |
Yan Liao Verena Vogel Sabine Hauber Jürgen Bartel Omer S. Alkhnbashi Sandra Maaß Thandi S. Schwarz Rolf Backofen Dörte Becher Iain G. Duggin Anita Marchfelder |
author_sort |
Yan Liao |
title |
CdrS Is a Global Transcriptional Regulator Influencing Cell Division in <named-content content-type="genus-species">Haloferax volcanii</named-content> |
title_short |
CdrS Is a Global Transcriptional Regulator Influencing Cell Division in <named-content content-type="genus-species">Haloferax volcanii</named-content> |
title_full |
CdrS Is a Global Transcriptional Regulator Influencing Cell Division in <named-content content-type="genus-species">Haloferax volcanii</named-content> |
title_fullStr |
CdrS Is a Global Transcriptional Regulator Influencing Cell Division in <named-content content-type="genus-species">Haloferax volcanii</named-content> |
title_full_unstemmed |
CdrS Is a Global Transcriptional Regulator Influencing Cell Division in <named-content content-type="genus-species">Haloferax volcanii</named-content> |
title_sort |
cdrs is a global transcriptional regulator influencing cell division in <named-content content-type="genus-species">haloferax volcanii</named-content> |
publisher |
American Society for Microbiology |
publishDate |
2021 |
url |
https://doaj.org/article/345d5fd461e344c58138b48125185e8b |
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