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...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: 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
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://doaj.org/article/345d5fd461e344c58138b48125185e8b
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:345d5fd461e344c58138b48125185e8b
record_format dspace
spelling 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)
institution DOAJ
collection DOAJ
language EN
topic Archaea
Haloferax volcanii
cell division
small protein
transcriptional regulation
Microbiology
QR1-502
spellingShingle 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
work_keys_str_mv AT yanliao cdrsisaglobaltranscriptionalregulatorinfluencingcelldivisioninnamedcontentcontenttypegenusspecieshaloferaxvolcaniinamedcontent
AT verenavogel cdrsisaglobaltranscriptionalregulatorinfluencingcelldivisioninnamedcontentcontenttypegenusspecieshaloferaxvolcaniinamedcontent
AT sabinehauber cdrsisaglobaltranscriptionalregulatorinfluencingcelldivisioninnamedcontentcontenttypegenusspecieshaloferaxvolcaniinamedcontent
AT jurgenbartel cdrsisaglobaltranscriptionalregulatorinfluencingcelldivisioninnamedcontentcontenttypegenusspecieshaloferaxvolcaniinamedcontent
AT omersalkhnbashi cdrsisaglobaltranscriptionalregulatorinfluencingcelldivisioninnamedcontentcontenttypegenusspecieshaloferaxvolcaniinamedcontent
AT sandramaaß cdrsisaglobaltranscriptionalregulatorinfluencingcelldivisioninnamedcontentcontenttypegenusspecieshaloferaxvolcaniinamedcontent
AT thandisschwarz cdrsisaglobaltranscriptionalregulatorinfluencingcelldivisioninnamedcontentcontenttypegenusspecieshaloferaxvolcaniinamedcontent
AT rolfbackofen cdrsisaglobaltranscriptionalregulatorinfluencingcelldivisioninnamedcontentcontenttypegenusspecieshaloferaxvolcaniinamedcontent
AT dortebecher cdrsisaglobaltranscriptionalregulatorinfluencingcelldivisioninnamedcontentcontenttypegenusspecieshaloferaxvolcaniinamedcontent
AT iaingduggin cdrsisaglobaltranscriptionalregulatorinfluencingcelldivisioninnamedcontentcontenttypegenusspecieshaloferaxvolcaniinamedcontent
AT anitamarchfelder cdrsisaglobaltranscriptionalregulatorinfluencingcelldivisioninnamedcontentcontenttypegenusspecieshaloferaxvolcaniinamedcontent
_version_ 1718439766243934208