DNA topoisomerase VIII: A novel subfamily of type IIB topoisomerases encoded by free or integrated plasmids in Archaea and Bacteria

Nucleic Acids Research

Volumn 42, Issue 13, 2014, Pages 8578-8591

  Gadelle, Danièle ^a   Krupovic, Mart ^b   Raymann, Kasie ^b   Mayer, Claudine ^b,c,d   Forterre, Patrick ^a,b  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b INSTITUT PASTEUR   (France)

^c CNRS   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA TOPOISOMERASE; DNA TOPOISOMERASE VIII; UNCLASSIFIED DRUG;

AMMONIFEX DEGENSII; ARCHAEON; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIUM; BACTEROIDETES; CLASSIFICATION; COMPUTER MODEL; DNA CLEAVAGE; ENZYME ACTIVITY; ENZYME STRUCTURE; FIRMICUTES; GENE IDENTIFICATION; GENETIC VARIABILITY; MICROSCILLA MARINA; NONHUMAN; PAENIBACILLUS ALVEI; PAENIBACILLUS POLYMYXA; PHYLOGENY; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOBACTERIA; RHIZOBIUM GALLICUM; ROSEOBACTER;

AMINO ACID SEQUENCE; ARCHAEA; ARCHAEAL PROTEINS; BACTERIA; BACTERIAL PROTEINS; CONSERVED SEQUENCE; DNA TOPOISOMERASES; GENOME, BACTERIAL; PHYLOGENY; PLASMIDS;

EID: 84905572229     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku568     Document Type: Article

References (68)

1. Schoeffler, A.J. and Berger, J.M. Schoeffler, A.J. and Berger, J.M. (2008) Topos: harnessing and constraining energy to govern chromosome topology. Q. Rev. Biophys., 41, 41-101.
2. Wang, J.C. Wang, J.C. (2009) In: Untangling the Double Helix, Cold Spring Harbor Laboratory Press, Harvard University..
3. Forterre, P. Pommier, YEd. Forterre, P. Inedpp. Forterre, P. (2011) Introduction and historical perspective. In:Topos and Cancer , Pommier, YEd. Humana press, Springer-Verlag. pp. 1-52.
4. Bergerat, A., de Massy, B., Gadelle, D., Varoutas, P.C., Nicolas, A., and Forterre, P. Bergerat, A., de Massy, B., Gadelle, D., Varoutas, P.C., Nicolas, A., and Forterre, P. (1997) An atypical topoisomerases II from Archaea with implications for meiotic recombination. Nature, 386, 414-417.
5. Gadelle, D., Filée, J., Buhler, C., and Forterre, P. Gadelle, D., Filée, J., Buhler, C., and Forterre, P. (2003) Phylogenomics of type II Topos. Bioessays, 25, 232-242.
6. Corbett, K.D. and Berger, J.M. Corbett, K.D. and Berger, J.M. (2004) Structure, molecular mechanisms, and evolutionary relationships in Topos. Annu. Rev. Biophys. Biomol. Struct., 33, 95-118.
7. Forterre, P. and Gadelle, D. Forterre, P. and Gadelle, D. (2009) Phylogenomics of Topos: their origin and putative roles in the emergence of modern organisms. Nucleic Acids Res., 37, 679-692.
8. Schoeffler, A.J. and Berger, J.M. Schoeffler, A.J. and Berger, J.M. (2005) Recent advances in understanding structure-function relationships in the type II topoisomerases mechanism. Biochem. Soc. Trans., 33, 1465-1470.
9. Corbett, K.D., Benedetti, P., and Berger, J.M. Corbett, K.D., Benedetti, P., and Berger, J.M. (2007) Holoenzyme assembly and ATP-mediated conformational dynamics of topoisomerases VI. Nat. Struct. Mol. Biol., 14, 611-619.
10. Graille, M., Cladière, L., Durand, D., Lecointe, F., Gadelle, D., Quevillon-Cheruel, S., Vachette, P., Forterre, P., and van Tilbeurgh, H. Graille, M., Cladière, L., Durand, D., Lecointe, F., Gadelle, D., Quevillon-Cheruel, S., Vachette, P., Forterre, P., and van Tilbeurgh, H. (2008) Crystal structure of an intact type II Topos: insights into DNA transfer mechanisms. Structure, 16, 360-370.
11. Laponogov, I., Sohi, M.K., Veselkov, D.A., Pan, X.-S., Sawhney, R., Thompson, A.W., McAuley, K.E., Fisher, L.M., and Sanderson, M.R. Laponogov, I., Sohi, M.K., Veselkov, D.A., Pan, X.-S., Sawhney, R., Thompson, A.W., McAuley, K.E., Fisher, L.M., and Sanderson, M.R. (2009) Structural insight into the quinolone-DNA cleavage complex of type IIA topoisomerases. Nat. Struct. Mol. Biol., 16, 667-669.
12. Dutta, R. and Inouye, M. Dutta, R. and Inouye, M. (2000) GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci., 25, 24-28.
13. Woese, C.R., Kandler, O., and Wheelis, M.L. Woese, C.R., Kandler, O., and Wheelis, M.L. (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. U.S.A., 87, 4576-4579.
14. Lecompte, O., Ripp, R., Thierry, J.-C., Moras, D., and Poch, O. Lecompte, O., Ripp, R., Thierry, J.-C., Moras, D., and Poch, O. (2002) Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale. Nucleic Acids Res., 30, 5382-5390.
15. Forterre, P., Gribaldo, S., Gadelle, D., and Serre, M.-C. Forterre, P., Gribaldo, S., Gadelle, D., and Serre, M.-C. (2007) Origin and evolution of Topos. Biochimie, 89, 427-446.
16. Bergerat, A., Gadelle, D., and Forterre, P. Bergerat, A., Gadelle, D., and Forterre, P. (1994) Purification of a Topos II from the hyperthermophilic archaeon Sulfolobus shibatae. A thermostable enzyme with both bacterial and eucaryal features. J. Biol. Chem., 269, 27 663-27 669.
17. Brochier-Armanet, C., Gribaldo, S., and Forterre, P. Brochier-Armanet, C., Gribaldo, S., and Forterre, P. (2008) A Topos IB in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of Archaea and Eucarya. Biol. Direct, 3, 54.
18. Sugimoto-Shirasu, K., Stacey, N.J., Corsar, J., Roberts, K., and McCann, M.C. Sugimoto-Shirasu, K., Stacey, N.J., Corsar, J., Roberts, K., and McCann, M.C. (2002) Topos VI is essential for endoreduplication in Arabidopsis. Curr. Biol., 12, 1782-1786.
19. Filée, J., Forterre, P., Sen-Lin, T., and Laurent, J. Filée, J., Forterre, P., Sen-Lin, T., and Laurent, J. (2002) Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins. J. Mol. Evol., 54, 763-773.
20. Forterre, P. Forterre, P. (2002) The origin of DNA genomes and DNA replication proteins. Curr. Opin. Microbiol., 5, 525-532.
21. Plewniak, F., Bianchetti, L., Brelivet, Y., Carles, A., Chalmel, F., Lecompte, O., Mochel, T., Moulinier, L., Muller, A., and Muller, J. et al. Plewniak, F., Bianchetti, L., Brelivet, Y., Carles, A., Chalmel, F., Lecompte, O., Mochel, T., Moulinier, L., Muller, A., and Muller, J. (2003) PipeAlign: A new toolkit for protein family analysis. Nucleic Acids Res., 31, 3829-3832.
22. Jones, D.T. Jones, D.T. (1999) Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol., 292, 195-202.
23. Edgar, R.C. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797.
24. Gouy, M., Guindon, S., and Gascuel, O. Gouy, M., Guindon, S., and Gascuel, O. (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol., 27, 221-224.
25. Criscuolo, A. and Gribaldo, S. Criscuolo, A. and Gribaldo, S. (2010) BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol., 10, 210.
26. Abascal, F., Zardoya, R., and Posada, D. Abascal, F., Zardoya, R., and Posada, D. (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics, 21, 2104-2105.
27. Stamatakis, A. Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688-2690.
28. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A., and Huelsenbeck, J.P. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A., and Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol., 61, 539-542.
29. Kelley, L.A. and Sternberg, M.J.E. Kelley, L.A. and Sternberg, M.J.E. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc., 4, 363-371.
30. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics, 22, 195-201.
31. Krupovic, M., Forterre, P., and Bamford, D.H. Krupovic, M., Forterre, P., and Bamford, D.H. (2010) Comparative analysis of the mosaic genomes of tailed archaeal viruses and proviruses suggests common themes for virion architecture and assembly with tailed viruses of bacteria. J. Mol. Biol., 397, 144-160.
32. Krumsiek, J., Arnold, R., and Rattei, T. Krumsiek, J., Arnold, R., and Rattei, T. (2007) Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics, 23, 1026-1028.
33. Bizard, A., Garnier, F., and Nadal, M. Bizard, A., Garnier, F., and Nadal, M. (2011) TopR2, the second reverse gyrase of Sulfolobus solfataricus, exhibits unusual properties. J. Mol. Biol., 408, 839-849.
34. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
35. Krupovic, M., Gribaldo, S., Bamford, D.H., and Forterre, P. Krupovic, M., Gribaldo, S., Bamford, D.H., and Forterre, P. (2010) The evolutionary history of archaeal MCM helicases: a case study of vertical evolution combined with hitchhiking of mobile genetic elements. Mol. Biol. Evol., 27, 2716-2732.
36. Soler, N., Marguet, E., Cortez, D., Desnoues, N., Keller, J., van Tilbeurgh, H., Sezonov, G., and Forterre, P. Soler, N., Marguet, E., Cortez, D., Desnoues, N., Keller, J., van Tilbeurgh, H., Sezonov, G., and Forterre, P. (2010) Two novel families of plasmids from hyperthermophilic archaea encoding new families of replication proteins. Nucleic Acids Res., 38, 5088-5104.
37. Forterre, P. Forterre, P. (2012) Darwin's goldmine is still open: variation and selection run the world. Front. Cell Infect. Microbiol., 2, 106.
38. Raymann, K., Forterre, P., Brochier-Armanet, C., and Gribaldo, S.doi:10.1093/gbe/evu004Raymann, K., Forterre, P., Brochier-Armanet, C., and Gribaldo, S. (2014) Genome Biol. Evol.,.
39. Wozniak, R.A.F. and Waldor, M.K. Wozniak, R.A.F. and Waldor, M.K. (2010) Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat. Rev. Microbiol., 8, 552-563.
40. Lipps, G. Lipps, G. (2004) The replication protein of the Sulfolobus islandicus plasmid pRN1. Biochem. Soc. Trans., 32, 240-244.
41. Krupovic, M., Gonnet, M., Hania, W.B., Forterre, P., and Erauso, G. Krupovic, M., Gonnet, M., Hania, W.B., Forterre, P., and Erauso, G. (2013) Insights into dynamics of mobile genetic elements in hyperthermophilic environments from five new Thermococcus plasmids. PLoS One, 8, e49044.
42. Gill, S., Krupovic, M., Desnoues, N., Béguin, P., Sezonov, G., and Forterre, P. Gill, S., Krupovic, M., Desnoues, N., Béguin, P., Sezonov, G., and Forterre, P. (2014) A highly divergent archaeo-eukaryotic primase from the Thermococcus nautilus plasmid, pTN2. Nucleic Acids Res., 42, 3707-3719.
43. Gornik, S.G., Ford, K.L., Mulhern, T.D., Bacic, A., McFadden, G.I., and Waller, R.F. Gornik, S.G., Ford, K.L., Mulhern, T.D., Bacic, A., McFadden, G.I., and Waller, R.F. (2012) Loss of nucleosomal DNA condensation coincides with appearance of a novel nuclear protein in dinoflagellates. Curr. Biol., 22, 2303-2312.
44. Filée, J. and Forterre, P. Filée, J. and Forterre, P. (2005) Viral proteins functioning in organelles: a cryptic origin. Trends Microbiol., 13, 510-513.
45. Lal, S., Romano, S., Chiarini, L., Signorini, A., and Tabacchioni, S. Lal, S., Romano, S., Chiarini, L., Signorini, A., and Tabacchioni, S. (2012) The Paenibacillus polymyxa species is abundant among hydrogen-producing facultative anaerobic bacteria in Lake Averno sediment. Arch. Microbiol., 194, 345-351.
46. Huber, R., Rossnagel, P., Woese, C.R., Rachel, R., Langworthy, T.A., and Stetter, K.O. Huber, R., Rossnagel, P., Woese, C.R., Rachel, R., Langworthy, T.A., and Stetter, K.O. (1996) Formation of ammonium from nitrate during chemolithoautotrophic growth of the extremely thermophilic bacterium ammonifex degensii gen. nov. sp. nov. Syst. Appl. Microbiol., 19, 40-49.
47. Lewin, R.A. Lewin, R.A. (1969) A classification of flexibacteria. J. Gen. Microbiol., 58, 189-206.
48. Buhler, C., Gadelle, D., Forterre, P., Wang, J.C., and Bergerat, A. Buhler, C., Gadelle, D., Forterre, P., Wang, J.C., and Bergerat, A. (1998) Reconstitution of DNA topoisomerase VI of the thermophilic archaeon Sulfolobus shibatae from subunits separately overexpressed in Escherichia coli. Nucleic Acids Res., 26, 5157-62.
49. McClendon, A.K., Rodriguez, A.C., and Osheroff, N. McClendon, A.K., Rodriguez, A.C., and Osheroff, N. (2005) Human topoisomerase IIalpha rapidly relaxes positively supercoiled DNA: implications for enzyme action ahead of replication forks. J. Biol. Chem., 280, 39 337-45.
50. Aubry, A., Fisher, L.M., Jarlier, V., and Cambau, E. Aubry, A., Fisher, L.M., Jarlier, V., and Cambau, E. (2006) First functional characterization of a singly expressed bacterial type II topoisomerase: the enzyme from Mycobacterium tuberculosis. Biochem. Biophys. Res. Commun., 348, 158-65.
51. Matrat, S., Petrella, S., Cambau, E., Sougakoff, W., Jarlier, V., and Aubry, A. Matrat, S., Petrella, S., Cambau, E., Sougakoff, W., Jarlier, V., and Aubry, A. (2007) Expression and purification of an active form of the Mycobacterium leprae DNA gyrase and its inhibition by quinolones. Antimicrob. Agents Chemother., 51, 643-8.
52. Gellert, M., Mizuuchi, K., O'Dea, M.H., Itoh, T., and Tomizawa, J.I. Gellert, M., Mizuuchi, K., O'Dea, M.H., Itoh, T., and Tomizawa, J.I. (1977) Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity. Proc. Natl. Acad. Sci. U.S.A., 74, 4772-4776.
53. Sugino, A., Peebles, C.L., Kreuzer, K.N., and Cozzarelli, N.R. Sugino, A., Peebles, C.L., Kreuzer, K.N., and Cozzarelli, N.R. (1977) Mechanism of action of nalidixic acid: purification of Escherichia coli nalA gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme. Proc. Natl. Acad. Sci. U.S.A., 74, 4767-71.
54. Bates, A.D., Berger, J.M., and Maxwell, A. Bates, A.D., Berger, J.M., and Maxwell, A. (2011) The ancestral role of ATP hydrolysis in type II topoisomerases: prevention of DNA double-strand breaks. Nucleic Acids Res., 39, 6327-6339.
55. Kirik, V., Schrader, A., Uhrig, J.F., and Hulskamp, M. Kirik, V., Schrader, A., Uhrig, J.F., and Hulskamp, M. (2007) MIDGET unravels functions of the Arabidopsis topoisomerase VI complex in DNA endoreduplication, chromatin condensation, and transcriptional silencing. Plant Cell, 19, 3100-10.
56. Hayama, R. and Marians, K.J. Hayama, R. and Marians, K.J. (2010) Physical and functional interaction between the condensin MukB and the decatenase topoisomerase IV in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A., 107, 18826-18831.
57. Chikamori, K., Grozav, A.G., Kozuki, T., Grabowski, D., Ganapathi, R., and Ganapathi, M.K. Chikamori, K., Grozav, A.G., Kozuki, T., Grabowski, D., Ganapathi, R., and Ganapathi, M.K. (2010) DNA topoisomerase II enzymes as molecular targets for cancer chemotherapy. Curr. Cancer Drug Targets, 10, 758-71.
58. Taneja, B., Patel, A., Slesarev, A., and Mondragón, A. Taneja, B., Patel, A., Slesarev, A., and Mondragón, A. (2006) Structure of the N-terminal fragment of topoisomerases V reveals a new family of topoisomerases. EMBO J., 25, 398-408.
59. Forterre, P. Forterre, P. (2006) Topos V: a new fold of mysterious origin. Trends Biotechnol., 24, 245-247.
60. Forterre, P. Forterre, P. (2005) The two ages of the RNA world, and the transition to the DNA world: a story of viruses and cells. Biochimie, 87, 793-803.
61. Koonin, E.V. and Dolja, V.V. Koonin, E.V. and Dolja, V.V. (2013) A virocentric perspective on the evolution of life. Curr. Opin. Virol., 3, 546-557.
62. Krupovic, M. Krupovic, M. (2013) Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses. Curr. Opin. Virol., 3, 578-586.
63. Nelson-Sathi, S., Dagan, T., Landan, G., Janssen, A., Steel, M., McInerney, J.O., Deppenmeier, U., and Martin, W.F. Nelson-Sathi, S., Dagan, T., Landan, G., Janssen, A., Steel, M., McInerney, J.O., Deppenmeier, U., and Martin, W.F. (2012) Acquisition of 1, 000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea. Proc. Natl. Acad. Sci. U.S.A., 109, 20 537-20 542.
64. Kolkenbrock, S., Naumann, B., Hippler, M., and Fetzner, S. Kolkenbrock, S., Naumann, B., Hippler, M., and Fetzner, S. (2010) A novel replicative enzyme encoded by the linear Arthrobacter plasmid pAL1. J. Bacteriol., 192, 4935-4943.
65. Li, Z., Hiasa, H., Kumar, U., and DiGate, R.J. Li, Z., Hiasa, H., Kumar, U., and DiGate, R.J. (1997) The traE gene of plasmid RP4 encodes a homologue of Escherichia coli Topos III. J. Biol. Chem., 272, 19 582-19 587.
66. Lee, S.-H., Siaw, G.E.-L., Willcox, S., Griffith, J.D., and Hsieh, T.-S. Lee, S.-H., Siaw, G.E.-L., Willcox, S., Griffith, J.D., and Hsieh, T.-S. (2013) Synthesis and dissolution of hemicatenanes by type IA Topos. Proc. Natl. Acad. Sci. U.S.A., 110, E3587-94.
67. Niu, B., Rueckert, C., Blom, J., Wang, Q., and Borriss, R. Niu, B., Rueckert, C., Blom, J., Wang, Q., and Borriss, R. (2011) The genome of the plant growth-promoting rhizobacterium Paenibacillus polymyxa M-1 contains nine sites dedicated to nonribosomal synthesis of lipopeptides and polyketides. J. Bacteriol., 193, 5862-5863.
68. Vetting, M.W., Hegde, S.S., Wang, M., Jacoby, G.A., Hooper, D.C., and Blanchard, J.S. Vetting, M.W., Hegde, S.S., Wang, M., Jacoby, G.A., Hooper, D.C., and Blanchard, J.S. (2011) Structure of QnrB1, a plasmid-mediated fluoroquinolone resistance factor. J. Biol. Chem., 286, 25265-25273.