Insights into synthesis and function of KsgA/Dim1-dependent rRNA modifications in archaea.


Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
22 02 2021
Historique:
accepted: 21 12 2020
revised: 01 12 2020
received: 28 10 2020
pubmed: 13 1 2021
medline: 4 3 2021
entrez: 12 1 2021
Statut: ppublish

Résumé

Ribosomes are intricate molecular machines ensuring proper protein synthesis in every cell. Ribosome biogenesis is a complex process which has been intensively analyzed in bacteria and eukaryotes. In contrast, our understanding of the in vivo archaeal ribosome biogenesis pathway remains less characterized. Here, we have analyzed the in vivo role of the almost universally conserved ribosomal RNA dimethyltransferase KsgA/Dim1 homolog in archaea. Our study reveals that KsgA/Dim1-dependent 16S rRNA dimethylation is dispensable for the cellular growth of phylogenetically distant archaea. However, proteomics and functional analyses suggest that archaeal KsgA/Dim1 and its rRNA modification activity (i) influence the expression of a subset of proteins and (ii) contribute to archaeal cellular fitness and adaptation. In addition, our study reveals an unexpected KsgA/Dim1-dependent variability of rRNA modifications within the archaeal phylum. Combining structure-based functional studies across evolutionary divergent organisms, we provide evidence on how rRNA structure sequence variability (re-)shapes the KsgA/Dim1-dependent rRNA modification status. Finally, our results suggest an uncoupling between the KsgA/Dim1-dependent rRNA modification completion and its release from the nascent small ribosomal subunit. Collectively, our study provides additional understandings into principles of molecular functional adaptation, and further evolutionary and mechanistic insights into an almost universally conserved step of ribosome synthesis.

Identifiants

pubmed: 33434266
pii: 6090297
doi: 10.1093/nar/gkaa1268
pmc: PMC7897474
doi:

Substances chimiques

RNA, Archaeal 0
RNA, Ribosomal 0
Methyltransferases EC 2.1.1.-
16S rRNA (adenine(1518)-N(6)-adenine(1519)-N(6))-dimethyltransferase EC 2.1.1.182

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1662-1687

Subventions

Organisme : CIHR
ID : PJT 386315
Pays : Canada

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of Nucleic Acids Research.

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Auteurs

Robert Knüppel (R)

Regensburg Center for Biochemistry, Biochemistry III - Institute for Biochemistry, Genetics and Microbiology, University of Regensburg, Universitätsstraße 31, 93053 Regensburg, Germany.

Christian Trahan (C)

Institut de Recherches Cliniques de Montréal, 110 Avenue des Pins Ouest, Montréal, Québec H2W 1R7, Canada.
Faculty of Medicine, Division of Experimental Medicine, McGill University, Montréal, Québec H3A 1A3, Canada.
Département de Biochimie, Faculté de Médecine, Université de Montréal, Montréal, Québec H3T 1J4, Canada.

Michael Kern (M)

Regensburg Center for Biochemistry, Biochemistry III - Institute for Biochemistry, Genetics and Microbiology, University of Regensburg, Universitätsstraße 31, 93053 Regensburg, Germany.

Alexander Wagner (A)

Molecular Biology of Archaea, Institute of Biology II, Faculty of Biology, Microbiology, University of Freiburg, Freiburg, Germany.

Felix Grünberger (F)

Chair of Microbiology - Institute for Biochemistry, Genetics and Microbiology, University of Regensburg, Universitätsstraße 31, 93053 Regensburg, Germany.

Winfried Hausner (W)

Chair of Microbiology - Institute for Biochemistry, Genetics and Microbiology, University of Regensburg, Universitätsstraße 31, 93053 Regensburg, Germany.

Tessa E F Quax (TEF)

Archaeal Virus-Host Interactions, Institute of Biology II, Faculty of Biology, Microbiology, University of Freiburg, Freiburg, Germany.

Sonja-Verena Albers (SV)

Molecular Biology of Archaea, Institute of Biology II, Faculty of Biology, Microbiology, University of Freiburg, Freiburg, Germany.

Marlene Oeffinger (M)

Institut de Recherches Cliniques de Montréal, 110 Avenue des Pins Ouest, Montréal, Québec H2W 1R7, Canada.
Faculty of Medicine, Division of Experimental Medicine, McGill University, Montréal, Québec H3A 1A3, Canada.
Département de Biochimie, Faculté de Médecine, Université de Montréal, Montréal, Québec H3T 1J4, Canada.

Sébastien Ferreira-Cerca (S)

Regensburg Center for Biochemistry, Biochemistry III - Institute for Biochemistry, Genetics and Microbiology, University of Regensburg, Universitätsstraße 31, 93053 Regensburg, Germany.

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