Abstract
Some restriction–modification systems contain two DNA methyltransferases. In the present work, we have classified such systems according to the families of catalytic domains present in the restriction endonucleases and both DNA methyltransferases. Evolution of the restriction–modification systems containing an endonuclease with a NOV_C family domain and two DNA methyltransferases, both with DNA_methylase family domains, was investigated in detail. Phylogenetic tree of DNA methyltransferases from the systems of this class consists of two clades of the same size. Two DNA methyltransferases of each restriction–modification system of this class belong to the different clades. This indicates independent evolution of the two methyltransferases. We detected multiple cross-species horizontal transfers of the systems as a whole, as well as the cases of gene transfer between the systems.
Abbreviations
- HGT:
-
horizontal gene transfer
- MTase:
-
DNA-methyltransferase
- REase:
-
restriction endonuclease
- RM systems:
-
restriction–modification systems
References
Williams, R. J. (2003) Restriction endonucleases: classification, properties, and applications, Mol. Biotechnol., 23, 225-244, https://doi.org/10.1385/mb:23:3:225.
Roberts, R. J. (2003) A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes, Nucleic Acids Res., 31, 1805-1812, https://doi.org/10.1093/nar/gkg274.
Pingoud, A., Wilson, G. G., and Wende, W. (2014) Type II restriction endonucleases – a historical perspective and more, Nucleic Acids Res., 42, 7489-7527, https://doi.org/10.1093/nar/gku447.
Szybalski, W., Kim, S. C., Hasan, N., and Podhajska, A. J. (1991) Class-IIS restriction enzymes – a review, Gene, 100, 13-26, https://doi.org/10.1016/0378-1119(91)90345-c.
Madhusoodanan, U. K., and Rao, D. N. (2010) Diversity of DNA methyltransferases that recognize asymmetric target sequences, Crit. Rev. Biochem. Mol. Biol., 45, 125-145, https://doi.org/10.3109/10409231003628007.
Vasu, K., and Nagaraja, V. (2013) Diverse functions of restriction-modification systems in addition to cellular defense, Microbiol. Mol. Biol. Rev., 77, 53-72, https://doi.org/10.1128/mmbr.00044-12.
Furmanek-Blaszk, B., Boratynski, R., Zolcinska, N., and Sektas, M. (2009) M1.MboII and M2.MboII type IIS methyltransferases: Different specificities, the same target, Microbiology, 155, 1111-1121, https://doi.org/10.1099/mic.0.025023-0.
Kriukiene, E., Lubiene, J., Lagunavicius, A., and Lubys, A. (2005) MnlI – The member of H-N-H subtype of Type IIS restriction endonucleases, Biochim. Biophys. Acta, 1751, 194-204, https://doi.org/10.1016/j.bbapap.2005.06.006.
Sapranauskas, R., Sasnauskas, G., Lagunavicius, A., Vilkaitis, G., Lubys, A., and Siksnys, V. (2000) Novel subtype of type IIS restriction enzymes, J. Biol. Chem., 275, 30878-30885, https://doi.org/10.1074/jbc.m003350200.
Sugisaki, H., Kita, K., and Takanami, M. (1989) The FokI restriction-modification system, J. Biol. Chem., 264, 5757-5761, https://doi.org/10.1016/s0021-9258(18)83614-6.
Mistry, J., Chuguransky, S., Williams, L., Qureshi, M., Salazar, G. A., Sonnhammer, E. L. L., Tosatto, S. C. E., Paladin, L., Raj, S., Richardson, L. J., Finn, R. D., and Bateman, A. (2020) Pfam: The protein families database in 2021, Nucleic Acids Res., 49, D412-D419, https://doi.org/10.1093/nar/gkaa913.
Roberts, R. J., Vincze, T., Posfai, J., and Macelis, D. (2014) REBASE – a database for DNA restriction and modification: Enzymes, genes and genomes, Nucleic Acids Res., 43, D298-D299, https://doi.org/10.1093/nar/gku1046.
Lemoine, F., Correia, D., Lefort, V., Dopplt-Azeroual, O., Mareuil, F., Coen-Boulakia, S., and Gascuel, O. (2019) NGPhylogeny.fr: new generation phylogenetic services for non-specialists, Nucleic Acids Research, 47, W260-W265, https://doi.org/10.1093/nar/gkz303.
Letunic, I., and Bork, P. (2021) Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation, Nucleic Acids Res., 49, W293-W296, https://doi.org/10.1093/nar/gkab301.
Li, W., and Godzik, A. (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences, Bioinformatics, 22, 1658-1659, https://doi.org/10.1093/bioinformatics/btl158.
Steczkiewicz, K., Muszewska, A., Knizewski, L., Rychlewski, L., and Ginalski, K. (2012) Sequence, structure and functional diversity of PD-(D/E)XK phosphodiesterase superfamily, Nucleic Acids Res., 40, 7016-7045, https://doi.org/10.1093/nar/gks382.
Sukackaite, R., Grazulis, S., Bochtler, M., and Siksnys, V. (2008) The recognition domain of the BpuJI restriction endonuclease in complex with cognate DNA at 1.3-Å resolution, J. Mol. Biol., 378, 1084-1093, https://doi.org/10.1016/j.jmb.2008.03.041.
Sukackaite, R., Lagunavicius, A., Stankevicius, K., Urbanke, C., Venclovas, Č., and Siksnys, V. (2007) Restriction endonuclease BpuJI specific for the 5′-CCCGT sequence is related to the archaeal Holliday junction resolvase family, Nucleic Acids Res., 35, 2377-2389, https://doi.org/10.1093/nar/gkm164.
Degtyarev, S. K., Netesova, N. A., Chizhikov, V. E., and Abdurashitov, M. (1998) Cloning and characterization of the gene encoding M.FauI DNA methyltransferase, Biol. Chem., 379, 567-568.
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This work was financially supported by the Russian Science Foundation (Grant no. 21-14-00135).
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A.V. Alekseevsky – concept and management of the work; A.S. Fokina – computer analysis of the data; I.S. Rusinov – preparation of the data on domains in REBASE proteins; D.M. Moshensky – assistance in searching for protein genes; A.S. Fokina, S.A. Spirin, A.S. Karyagina – discussion of the results, writing and editing of the article text.
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Fokina, A.S., Karyagina, A.S., Rusinov, I.S. et al. Evolution of Restriction–Modification Systems Consisting of One Restriction Endonuclease and Two DNA Methyltransferases. Biochemistry Moscow 88, 253–261 (2023). https://doi.org/10.1134/S0006297923020086
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DOI: https://doi.org/10.1134/S0006297923020086