Abstract
In silico analysis of open reading frames of genomic islands of Sinorhizobium meliloti Rm1021 was performed. This strain is a typical representative of soil bacteria forming nitrogen-fixing symbiosis with legume host plants from the alfalfa cross-inoculation group. It was demonstrated that genomic islands had mosaic structure, in which blocks of functional genes, IS-elements and noncoding RNA alternated. Genomic islands contained as well the components of T4SS and T4CP systems, and lacked systems of conjugative mobilization of islands. It was concluded that two of the three islands could be the variants of reduced integrative conjugative elements, and the third island represented a reduced integrated conjugative transposon. Site-specific integration of islands occurred into a 15–31 bp sequence (depending on the island) localized at the 3′-end of the tRNA gene, which is then shifted rightward, while the remaining part of the tRNA gene is completed by a similar sequence that exists in the island. A suggestion on the existence of “speciesspecific insertion hotspots” for genomic islands of root nodule bacteria was put forward.
Similar content being viewed by others
References
Sullivan, J.T., Trzebiatowski, J.R., Cruickshank, R.W., et al., Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A, J. Bacteriol., 2002, vol. 184, no. 11, pp. 3086–3095. doi 10.1128/JB.184.11.3086-3095.2002
Kaneko, T., Nakamura, Y., Sato, S., et al., Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110, DNA Res., 2002, vol. 9, no. 6, pp. 189–197. doi 10.1093/dnares/9.6.189
Leimbach, A., Hacker, J., and Dobrindt, U., E. coli as an all-rounder: the thin line between commensalism and pathogenicity, Curr. Top. Microbiol. Immunol., 2013, vol. 358, pp. 3–32. doi 10.1007/82_2012_303
Mavingui, P., Flores, M., Guo, X., et al., Dynamics of genome architecture in Rhizobium sp. strain NGR234, J. Bacteriol., 2002, vol. 184, no. 1, pp. 171–176. doi 10.1128/JB.184.1.171–176.2002
Gonzalez, J.M., Gomez-Puertas, P., Cavanagh, D., et al., A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae, Arch. Virol., 2003, vol. 148, no. 11, pp. 2207–2235. doi 10.1007/s00705-003-0162-1
Okubo, T., Piromyou, P., Tittabutr, P., et al., Origin and evolution of nitrogen fixation genes on symbiosis islands and plasmid in Bradyrhizobium, Microbes Environ., 2016, vol. 31, no. 3, pp. 260–267. doi 10.1264/jsme2.ME15159
Barcellos, F.G., Menna, P., Silva Batista, J.S., and Hungria, M., Evidence of horizontal transfer of symbiotic genes from a Bradyrhizobium japonicum inoculant strain to indigenous diazotrophs Sinorhizobium (Ensifer) fredii and Bradyrhizobium elkanii in a Brazilian savannah soil, Appl. Environ. Microbiol., 2007, vol. 73, no. 8, pp. 2635–2643. doi 10.1128/AEM.01823-06
Sullivan, J.T. and Ronson, C.W., Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene, Proc. Natl. Acad. Sci. U.S.A., 1998, vol. 95, no. 9, pp. 5145–5149.
Ramsay, J.P., Sullivan, J.T., Stuart, G.S., et al., Excision and transfer of the Mesorhizobium loti R7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS, Mol. Microbiol., 2006, vol. 62, no. 3, pp. 723–734. doi 10.1111/j.1365-2958.2006.05396.x
Haskett, T.L., Ramsa, J.P., Bekuma, A.A., et al., Evolutionary persistence of tripartite integrative and conjugative elements, Plasmid, 2017, vol. 92, pp. 30–36. doi 10.1016/j.plasmid.2017.06.001
Capela, D., Barloy-Hubler, F., Gouzy, J., et al., Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021, Proc. Natl. Acad. Sci. U.S.A., 2001, vol. 98, no. 17, pp. 9877–9882. doi 10.1073/pnas.161294398
Sibley, C.D., MacLellan, S.R., and Finan, T., The Sinorhizobium meliloti chromosomal origin of replication, Microbiology, 2006, vol. 152, pp. 443–455. doi 10.1099/mic.0.28455-0
Bellanger, X., Payot, S., Leblon-Bourget, N., and Guedon, G., Conjugative and mobilizable genomic islands in bacteria evolution and diversity, FEMS Microboil. Rev., 2014, vol. 1, no. 42, pp. 1–42. doi 10.1111/1574-6976.12058
Muntyan, V.S., Cherkasova, M.E., Andronov, E.E., et al., Occurrence of “islands” in genomes of Sinorhizobium meliloti native isolates, Russ. J. Genet., 2016, vol. 52, no. 10, pp. 1126–1133. doi 10.1134/S102279541608010X
Ulve, V.M., Sevin, E.W., Cheron, A., and Barloy-Hubler, F., Identification of chromosomal alpha-proteobacterial small RNAs by comparative genome analysis and detection in Sinorhizobium meliloti strain 1021, BMC Genomics, 2007, vol. 8:467. doi 10.1186/1471-2164-8-467
Barra-Bily, L., Pandey, S.P., Trautwetter, A., et al., The Sinorhizobium meliloti RNA chaperone Hfq mediates symbiosis of S. meliloti and alfalfa, J. Bacteriol., 2010, vol. 192, no. 6, pp. 1710–1718. doi 10.1128/JB.01427-09
Mahillon, J. and Chandler, M., Insertion sequences, Microbiol. Mol. Biol. Rev., 1998, vol. 62, no. 3, pp. 725–774.
Niemann, S., Puehler, A., Tichy, H.-V., et al., Evaluation of the resolving power of three different DNA fingerprinting methods to discriminate among isolates of a natural Rhizobium meliloti population, J. Appl. Microbiol., 1997, vol. 82, no. 4, pp. 477–484. doi 10.1046/j.1365-2672.1997.00141.x
Andronov, E.E., Roumiantseva, M.L., and Simarov, B.V., Genetic diversity of a natural population of Sinorhizobium meliloti revealed in analysis of cryptic plasmids and ISRm2011-2 fingerprints, Russ. J. Genet., 2001, vol. 37, no. 5, pp. 494–499. doi.org/. doi 10.1023/A:1016658429756
Roumiantseva, M.L., Yakutkina, V.V., Damman-Kalinovski, T., et al., Comparative analysis of structural organization of the genome in alfalfa nodule bacteria Sinorhizobium medicae and S. meliloti, Russ. J. Genet., 1999, vol. 35, no. 2, pp. 178–186.
Vasu, K. and Nagarajaa, V., Diverse functions of restriction-modification systems in addition to cellular defense, Microbiol. Mol. Biol., 2013, vol. 77, no. 1, pp. 53–72. doi 10.1128/MMBR.00044-12
Ravin, N.V. and Shestakov, S.V., Genome of Prokaryotes, Vavilovskii Zh. Genet. Sel., 2013, vol. 17, no. 4/2, pp. 972–984.
Tatusov, R.L., Galperin, M.Y., Natale, D.A., and Koonin, E.V., Using the COG database to improve gene recognition in complete genomes, Nucleic Acids Res., 2000, vol. 28, no. 1, pp. 33–36. doi 10.1023/A:1004031323748
Ferrieres, L., Francez-Charlot, A., Gouzy, J., et al., FixJ-regulated genes evolved through promoter duplication in Sinorhizobium meliloti, Microbiology, 2004, vol. 150, pp. 2335–2345. doi 10.1099/mic.0.27081-0
Bobik, C., Meilhoc, E., and Batut, J., FixJ: a major regulator of the oxygen limitation response and late symbiotic functions of Sinorhizobium meliloti, J. Bacteriol., 2006, vol. 188, no. 13, pp. 4890–4902. doi 10.1128/JB.00251-06
Demidenok, O.I. and Goncharenko, A.V., Toxin—antitoxin systems of bacteria and the prospects of their use in medicine (review), Prikl. Biokh. Mikrobiol., 2013, vol. 49, no. 6, pp. 539–546.
Il’inskaya, O.N. and Shakh Makhmud, R., Ribonucleases as antiviral agents, Mol. Biol. (Moscow), 2014, vol. 48, no. 5, pp. 615–623. doi 10.7868/S0026898414040053
Cook, G.M., Robson, J.R., Frampton, R.A., et al., Ribonucleases in bacterial toxin—antitoxin systems, Biochim. Biophys. Acta, 2013, vol. 1829, pp. 523–531. doi 10.1016/j.bbagrm.2013.02.007
Cho, J., Vergin, K., Morris, R., and Giovannoni, S., Lentisphaera araneosa gen. nov., sp. nov, a transparent exopolymer producing marine bacterium, and the description of a novel bacterial phylum, Lentisphaerae, Environ. Microbiol., 2004, vol. 6, no. 6, pp. 611–621. doi 10.1111/j.1462-2920.2004.00614.x
Hug, L.A., Baker, B.J., Anantharaman, K., et al., A new view of the tree of life, Nat. Microbiol., 2016. 1:16048. doi 10.1038/nmicrobiol.2016.48
Shestakov, S.V., How does the horizontal gene transfer in bacteria occur and how it is controlled, Ekol. Genet., 2007, vol. 5, no. 2, pp. 12–24.
Martinez-Hidalgo, P. and Hirsch, A.M., The nodule microbiome: N2-fixing rhizobia do not live alone, Phytobiomes, 2017, vol. 1, no. 2, pp. 70–82. doi 10.1094/PBIOMES-12-16-0019-RVW
Guo, X., Flores, M., Mavingui, P., et al., Natural genomic design in Sinorhizobium meliloti: novel genomic architectures, Genome Res., 2003, vol. 13, no. 8, pp. 1810–1817.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © M.L. Roumiantseva, V.S. Muntyan, M.E. Cherkasova, A.S. Saksaganskaya, E.E. Andronov, B.V. Simarov, 2018, published in Genetika, 2018, Vol. 54, No. 7.
Rights and permissions
About this article
Cite this article
Roumiantseva, M.L., Muntyan, V.S., Cherkasova, M.E. et al. Genomic Islands in Sinorhizobium meliloti Rm1021, Nitrogen-Fixing Symbiont of Alfalfa. Russ J Genet 54, 759–769 (2018). https://doi.org/10.1134/S102279541807013X
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S102279541807013X