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DNA Topoisomerase VIII DNA topoisomerase VIII: a novel subfamily of type IIB topoisomerases encoded by free or integrated plasmids in Archaea and Bacteria Danièle Gadelle, Mart Krupovic, Kasie Raymann, Claudine Mayer, Patrick Forterre To cite this version: Danièle Gadelle, Mart Krupovic, Kasie Raymann, Claudine Mayer, Patrick Forterre. DNA topoiso- merase VIII: a novel subfamily of type IIB topoisomerases encoded by free or integrated plasmids in Archaea and Bacteria. Nucleic Acids Research, Oxford University Press, 2014, 42 (13), pp.8578-8591. 10.1093/nar/gku568. pasteur-01977397 HAL Id: pasteur-01977397 https://hal-pasteur.archives-ouvertes.fr/pasteur-01977397 Submitted on 10 Jan 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. 8578–8591 Nucleic Acids Research, 2014, Vol. 42, No. 13 Published online 02 July 2014 doi: 10.1093/nar/gku568 DNA topoisomerase VIII: a novel subfamily of type IIB topoisomerases encoded by free or integrated plasmids in Archaea and Bacteria Daniele` Gadelle1, Mart Krupovic2, Kasie Raymann2, Claudine Mayer3,4,5 and Patrick Forterre1,2,* Downloaded from https://academic.oup.com/nar/article-abstract/42/13/8578/1293581 by Institut Pasteur user on 23 January 2019 1Universite´ Paris-Sud, CNRS UMR8621, Institut de Gen´ etique´ Microbiologie, 91405 Orsay Cedex, France, 2Institut Pasteur, Unite´ de Biologie moleculaire´ du gene` chez les extremophiles,ˆ Departement´ de Microbiologie, F-75015 Paris, France, 3Institut Pasteur, Unite´ de Microbiologie structurale, Departement´ de Biologie structurale et Chimie, F-75015 Paris, France, 4CNRS, UMR3528, F-75015 Paris, France and 5Universite´ Paris Diderot, Sorbonne Paris Cite,´ Cellule Pasteur, rue du Dr Roux 75015 Paris, France Received February 4, 2014; Revised June 10, 2014; Accepted June 11, 2014 ABSTRACT INTRODUCTION Type II DNA topoisomerases are divided into two fam- DNA topoisomerases are essential for solving topological ilies, IIA and IIB. Types IIA and IIB enzymes share problems arising during DNA metabolic processes and are homologous B subunits encompassing the ATP- therefore critical for the preservation of genome stability binding site, but have non-homologous A subunits (1–3). They can interconvert different topological forms of catalyzing DNA cleavage. Type IIA topoisomerases DNA and either catenate or decatenate DNA rings by gen- erating transient single- (type I topoisomerases) or double- are ubiquitous in Bacteria and Eukarya, whereas stranded (type II topoisomerases) DNA breaks in DNA members of the IIB family are mostly present in Ar- backbones. Type II enzymes are especially important be- chaea and plants. Here, we report the detection of cause of their unique capacity to catalyze the transfer of genes encoding type IIB enzymes in which the A and one DNA duplex through another. They are essential for B subunits are fused into a single polypeptide. These resolving catenanes generated between daughter chromo- proteins are encoded in several bacterial genomes, somes at the end of DNA replication and also play a ma- two bacterial plasmids and one archaeal plasmid. jor role in relaxing positive supercoils generated by track- They form a monophyletic group that is very diver- ing processes occurring during transcription and replica- gent from archaeal and eukaryotic type IIB enzymes tion. Accordingly, all cellular organisms, without exception, (DNA topoisomerase VI). We propose to classify them have at least one type II enzyme. into a new subfamily, denoted DNA topoisomerase Type II topoisomerases are classified into two families, IIA and IIB, based on sequence and structural similarities VIII. Bacterial genes encoding a topoisomerase VIII (4–7). Archaeal and bacterial types IIA and IIB enzymes are are present within integrated mobile elements, most heterotetramers composed of two different subunits (A and likely derived from conjugative plasmids. Purified B), whereas type IIA enzymes from eukaryotes and their topoisomerase VIII encoded by the plasmid pPPM1a viruses are homodimers, with the B and A moieties fused from Paenibacillus polymyxa M1 had ATP-dependent into a single polypeptide. Several high-resolution structures relaxation and decatenation activities. In contrast, of both types IIA and IIB enzymes have been solved, high- the enzyme encoded by mobile elements integrated lighting some structural similarities, but also large differ- into the genome of Ammonifex degensii exhibited ences between these two families (8–11). The B subunits DNA cleavage activity producing a full-length linear are homologous in the two families and contain a similar plasmid and that from Microscilla marina exhibited ATP-binding site located within a protein domain known as ATP-independent relaxation activity.Topoisomerases the Bergerat fold, which is characteristic of proteins of the GHKL (Gyrase, Hsp90, histidine Kinase, MutL) superfam- VIII, the smallest known type IIB enzymes, could be ily (4,12). Moreover, enzymes from the two families share new promising models for structural and mechanis- two other functional domains: the Toprim domain display- tic studies. ing the Rossmann fold (involved in magnesium binding) and *To whom correspondence should be addressed. Tel: +3369156445; Fax: +3369157808; Email: [email protected] C The Author(s) 2014. Published by Oxford University Press on behalf of Nucleic Acids Research. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by-nc/3.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] Nucleic Acids Research, 2014, Vol. 42, No. 13 8579 the Winged Helix Domain (WHD), which contains the ac- scenarios. We proposed previously that proteins involved in tive site tyrosine. However, the Toprim domain of type IIA DNA metabolic activities (including topoisomerases) origi- topoisomerases is located within the B subunit, whereas in nated first in the viral world and were later transferred ‘ran- the IIB family, this domain is located within the A subunit. domly’ to various cellular lineages (20). This scenario pre- Furthermore, their WHDs are unrelated, despite the pres- dicts that some contemporary viruses or related mobile ele- ence of the catalytic tyrosine in both cases (Figure 1). Over- ments (plasmids, transposons) still encode unique versions all, the A subunits of types IIA and IIB topoisomerases of DNA replication proteins, such as topoisomerases, that share neither sequence nor structural similarity. This sug- were never transferred to the ‘cellular world’ (except as in- gests that these two enzyme families originated indepen- tegrated mobile elements) (7). Downloaded from https://academic.oup.com/nar/article-abstract/42/13/8578/1293581 by Institut Pasteur user on 23 January 2019 dently via the association of homologous B subunits with Here, we report the in silico discovery and preliminary non homologous A subunits (5). biochemical characterization of a new DNA topoisomerase The origin and evolution of topoisomerases are rather subfamily that supports the prediction outlined above. The puzzling. Ribosomal proteins exist in three distinct ver- genes encoding these proteins correspond to the fusion of sions, corresponding to the three cellular domains, Archaea, the B and A subunits of type IIB topoisomerases. We iden- Bacteria and Eukarya (13,14); however, each topoisomerase tified these genes in 19 bacterial genomes and in three plas- family exists in several versions (hereafter called subfam- mids (two from bacteria and one from an archaeon). In ilies) that do not overlap with the three domains in phy- bacterial genomes, these genes are located within integrated logenomic analyses (5–7,15). In addition, several groups of mobile elements related to conjugative plasmids. We puri- viruses encode topoisomerases that are not related to those fied three members of this new subfamily of type IIB en- of their hosts but instead form monophyletic groups that zymes (that we propose to call topoisomerase VIII): one branch in between cellular domains in phylogenetic analy- from a mesophilic bacterium, one from a thermophilic bac- ses (5,7,15). terium and one from a bacterial plasmid. We show that Several distinct subfamilies of type IIA enzymes are the enzyme encoded by the bacterial plasmid exhibits ATP- known, which differ in catalytic activity and/or quater- dependent relaxation and decatenation activities, the hall- nary structure. These include (i) DNA gyrases, present mark of type II topoisomerases, whereas the other two in all bacteria, in some members of the archaeal phylum enzymes, encoded by integrated elements, exhibit DNA Euryarchaeota and in eukaryotes with endosymbionts of cleavage activity, producing DNA double-stranded breaks, cyanobacterial origin; (ii) topoisomerase IV enzymes, spe- and/or ATP-independent relaxation activity. cific to bacteria; (iii) eukaryotic type II topoisomerases, present in all
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