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Root nodule bacteria Sinorhizobium meliloti: Tolerance to salinity and bacterial genetic determinants

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Abstract

The theoretical and experimental data on salt tolerance of root nodule bacteria Sinorhizobium meliloti (Ensifer meliloti), an alfalfa symbiont, and on genetic determination of this feature are reviewed. Extensive data are provided on the genes affecting adaptation of proteobacteria and on the groups of genes with activity depending on the osmolarity of the medium. Structural and functional polymorphism of the bet genes involved in betaine synthesis and transport in S. meliloti is discussed. The phenotypic and genotypic polymorphism in 282 native rhizobial strains isolated from the centers of alfalfa diversity affected by aridity and salinity is discussed. The isolates from the Aral Sea area and northern Caucasus were shown to possess the betC gene represented by two types of alleles: the dominant Atype allele found in Rm1021 and the less common divergent Etype allele, which was revealed in regions at the frequencies of 0.35 and 0.48, respectively. In the isolates with the salt-tolerant phenotype, which were isolated from root nodules and subsequently formed less effective symbioses with alfalfa, the frequency of Etype alleles was 2.5 times higher. Analysis of the nucleotide and amino acid sequences of the Etype allele of the betC gene revealed that establishment of this allele in the population was a result of positive selection. It is concluded that diversification of the functionally diverse bet genes occurring in S. meliloti affects the salt tolerance and symbiotic effectiveness of rhizobia.

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References

  1. Flowers, T.J., Improving crop salt tolerance, J. Experim. Bot., 2004, vol. 55, no. 396, pp. 307–319.

    Article  CAS  Google Scholar 

  2. FAO. Food outlook. Global Market Analysis, 2007. http://www.fao.Food outlook.com

    Google Scholar 

  3. Souss, M., Santamaria, M., Ocana, A., and Lluch, C., Effects of salinity on protein and lipopolysaccharide pattern in a salttolerant strain of Mesorhizobium ciceri, J. Appl. Microbiol., 2001, vol. 90, no. 3, pp. 476–481.

    Article  Google Scholar 

  4. Zahran, H.H., Rhizobiumlegume symbiosis and nitro gen fixation under severe conditions and in an arid cli mate, Microbiol. Mol. Biol. Rev., 1999, vol. 63, no. 4, pp. 968–989.

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Dzyubenko, N.I., Chapurin, V.F., Bukhteeva, A.V., and Soskov, Yu.D., Mobilization and investigation of perennial fodder crops in view of N. Vavilov's heritage, Tr. Prikl. Bot. Gen. Select., 2007, vol. 164, pp. 153–163.

    Google Scholar 

  6. Lesins, K. and Lesins, I., Genus Medicago (Legumino sae), a taxogenetic study, Plant Ecol., 1982, pp. 50–92.

    Google Scholar 

  7. Small, E., Pollenovule patterns in tribe Trifolieae (Leguminosae), Plant Syst. Evol., 1988, vol. 160, nos. Iss. 3–4, pp. 195–205.

    Google Scholar 

  8. Shamsutdinov, Z.Sh., Methods for ecological restora tion of arid systems in the regions of grazing livestock sector, Stepnoi Byull. Novosib. Univ., 2002, vol. 11, pp. 21–26.

    Google Scholar 

  9. Stepanova, G.V., Muntyan, V.S., and Rumyantseva, M.L., Response of the new Agniya alfalfa variety to inoculation with root nodule bacteria, Adaptivnoe kormoproizvodstvo, 2013, no. 3(15), pp. 43–48. (Adaptive Forage Produc tion). http://www. adaptagro.ru

    Google Scholar 

  10. Kulkarni, S., Surange, S., and Nautiyal, C.S., Crossing the limits of Rhizobium existence in extreme condi tions, Curr. Microbiol., 2000, vol. 41, pp. 402–409.

    Article  CAS  PubMed  Google Scholar 

  11. Silva, C., Kan, F.L., and MartinezRomero, E., Popu lation genetic structure of Sinorhizobium meliloti and S. medicae isolated from nodules of Medicago spp. in Mexico, FEMS Microbiol. Ecol., 2007, vol. 60, pp. 477–489.

    Article  CAS  PubMed  Google Scholar 

  12. Eardly, B.D., Materon, L.A., Smith, N.H., Johnson, D.A., Rumbaugh, M.D., and Selander, R.K., Genetic structure of natural populations of the nitrogen fixing bacterium Rhizobium meliloti, Appl. Environ. Microbiol., 1990, vol. 56, pp. 187–194.

    CAS  PubMed Central  PubMed  Google Scholar 

  13. Wails, R.J., Wells, D.H., and Long, S.R., Analysis of differences between Sinorhizobium meliloti 1021 and 2011 strains using the host calcium spiking response, Mol. Plant–Microbe Interact., 2002, vol. 15, no. 12, pp. 1245–1252.

    Article  Google Scholar 

  14. Elboutahiri, N., ThamiAlami, I., and Udupa, S.M., Phenotypic and genetic diversity in Sinorhizobium meliloti and S. medicae from drought and salt affected regions of Morocco, BMC Microbiol., 2010, vol. 10, p. 15.

    Article  PubMed Central  PubMed  Google Scholar 

  15. Rangin, C., Brunel, B., CleyetMarel, J.C., Per rineau, M.M., and Bena, G., Effects of Medicago trun catula genetic diversity, rhizobial competition, and strain effectiveness on the diversity of a natural Sinorhizobium species community, Appl. Environ. Microbiol., 2008, vol. 74, no. 18, pp. 5653–5661.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Andronov, E.E., Rumiantseva, M.L., and Simarov, B.V., Genetic diversity of a natural population of Sinorhizo bium meliloti, detected during analysis of a cryptic plas mid and ISRm20112 fingerprints, Russ. J. Genet., 2001, vol. 37, no. 5, pp. 610–616.

    Article  CAS  Google Scholar 

  17. GubryRangin, C., Garcia, M., and Bena, G., Partner choice in Medicago truncatula–Sinorhizobium symbio sis, Proc. Biol. Sci., 2010, vol. 277, no. 1690, pp. 1947–1951.

    Article  Google Scholar 

  18. Ibragimova, M.V., Rumiantseva, M.L., Onishchuk, O.P., Belova, V.S., Kurchak, O.N., Andronov, E.E., Dzyu benko, N.I., and Simarov, B.V., Symbiosis between the nodule bacterium Sinorhizobium meliloti and alfalfa (Medicago sativa) under salinization conditions, Microbiology (Moscow), 2006, vol. 75, no. 1, pp. 77–81.

    Article  CAS  Google Scholar 

  19. Yurkov, A.P., Yakobi, L.M., Roumiantseva, M.L., and Stepanova, G.V., Capacity of alfalfa MIS1 line mutants for symbiosis formation with root nodule bac teria, Estestv. Tekhn. Nauki, 2012, no. 6, pp. 124–128.

    Google Scholar 

  20. Simarov, B.V. and Roumiantseva, M.L., Genetic approaches for establishing highly efficient effective, competitive symbioses between root nodule bacteria and alfalfa under impact of abiotic stress factors (salin ization), in Mat. Konf. “Orientirovannye fundamen tal’nye issledovaniya i ikh realizatsiya v APK Rossii” (Oriented Basic Research and Their Realization in the Russian AgroIndustrial Complex), St. Petersburg, 2008, pp.11–12.

    Google Scholar 

  21. Zahran, H.H., Rhizobia from wild legumes: diversity, taxonomy, ecology, nitrogen fixation and biotechnol ogy, J. Biotechnol., 2001, vol. 91. nos. 2–3. pp. 143–153.

    Article  CAS  PubMed  Google Scholar 

  22. Abdelmoumen, H., FilaliMaltouf, A., Neyra, M., Belabed, A., Missbah, El., and Idrissi, M., Effect of high salts concentrations on the growth of rhizobia and responses to added osmotica, J. Appl. Microbiol., 1999, vol. 86, pp. 889–898.

    Article  CAS  Google Scholar 

  23. Bena, G., Lyet, A., Huguet, T., and Olivieri, I., Medicago–Sinorhizobium symbiotic specificity evolution and the geographic expansion of Medicago, J. Evol. Biol., 2005, vol. 18, no. 6, pp. 1547–1558.

    Article  CAS  PubMed  Google Scholar 

  24. Wei, W., Jiang, J., Li, X., Wang, L., and Yang, S.S., Iso lation of saltsensitive mutants from Sinorhizobium meliloti and characterization of genes involved in salt tolerance, Lett. Appl. Microbiol., 2004, vol. 39, pp. 278–283.

    Article  CAS  PubMed  Google Scholar 

  25. Roumiantseva, M.L., Belova, V.S., Onishchuk, O.P., Andronov, E.E., Kurchak, O.N., Chizhevskaya, E.P., Rumyantseva, T.B., and Simarov, B.V., Polymorphism of the bet genes in Sinorhizobium meliloti strains from alfalfa genetic centers, Sel’skokhoz. Biol., 2011, no. 3, pp. 48–54.

    Google Scholar 

  26. Dogra, T., Priyadarshini, A., Kumar, A., and Kumar Singh, N., Identification of genes involved in salt tolerance and symbiotic nitrogen fixation in chick pea rhizobium Mesorhizobium ciceri Ca181, Symbiosis, 2013, vol. 61, pp. 135–143.

    Article  CAS  Google Scholar 

  27. Aguilar, O.M., Riva, O., and Peltzer, E., Analysis of Rhizobium etli and of its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversi fication, Proc. Natl. Acad. Sci. U. S. A., 2004, vol. 101, no. 37, pp. 13548–13553.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Roumiantseva, M.L. Genetic resources of nodule bac teria (review), Russ. J. Genet., 2009, vol. 45, no. 9, pp. 1013–1026.

    Article  CAS  Google Scholar 

  29. Vavilov, N.I., Centers of origin of cultivated plants, in Trudy po prikladnoi botanike, genetike i selektsii (Works on Applied Botany, Genetics, and Selection), Lenin grad: Tip. im. Gutenberga, 1926, vol. 16, no. 2, pp. 3–248.

    Google Scholar 

  30. Sinskaya, E.N., Ecological system for selection of fod der plants, in Prilozh. №62k Tr. po prikl. bot., gen. i sel (Suppl. no. 62 to Proc. Appl. Bot., Genet., Selct.), Leningrad: VIR, 1933.

    Google Scholar 

  31. Kumar, H., Arora, N.K., Kumar, V., and Maheshwari, D.K., Isolation, characterization and selection of salttolerantrhizobia nodulating Acacia catechu and Acacia nilotica, Symbiosis, 1999, vol. 26, pp. 279–288.

    Google Scholar 

  32. Boncompagni, E. and Poggi, M.C., and Le Rudulier, D., Occurrence of choline and glycine betaine uptake and metabolism in the family Rhizobiaceae and their roles in osmoprotection, Appl. Environ. Microbiol., 1999, vol. 65, pp. 2072–2077.

    CAS  PubMed Central  PubMed  Google Scholar 

  33. Boscari, A. Van de Sype, G., Le Rudulier, D., and Mandon, K., Overexpression of BetS, a Sinorhizobium meliloti highaffinity betaine transporter, in bacteroids from Medicago sativa nodules sustains nitrogen fixation during early salt stress adaptation, Mol. Plant–Microbe Interact., 2006, vol. 19, no. 8, pp. 896–903.

    Article  CAS  PubMed  Google Scholar 

  34. Roumyantseva, M.L., Andronov, E.E., Onichtchouk, O.P., Kurchak, O.N., Ibragimova, M.V., Dzubenko, N.I., Lindstroem, K., Priefer, U.B., Giuntini, E., Bazzicalupo, M., and Simarov, B.V., Sinorhizo bium isolates from saltaffected Aral Sea asin, 5th Eur. Nitrogen Fixation Conf., Norwich, 2002.

    Google Scholar 

  35. Young, J.P.W., Crossman, L.C., Johnston, A.W.B., Thomson, N.R., Ghazoui, Z.F., Hull, K.H., Wexler, M., Curson, A.R.J., Todd, J.D., Poole, P.S., Mauchline, T.H., East, A.K., Quail, M.A., Churcher, C., Arrowsmith, C., Cherevach, I., Chilling worth, T., Clarke, K., Cronin, A., Davis, P., Fraser, A., Hance, Z., Hauser, H., Jagels, K., Moule, S., Mungall, K., Norbertczak, H., Rabbinowitsch, E., Sanders, M., Simmonds, M., Whitehead, S., and Parkhill, J., The genome of Rhizobium leguminosarum has recognizable core and accessory components, Genome Biol., 2006, 7R34. doi: 10.1186/gb-2006-7-4-r34

    Google Scholar 

  36. Roumiantseva, M.L., Simarov, B.V., Onishchuk, O.P., Andronov, E.E., Chizhevskaya, E.P., Belova, V.S., Kurchak, O.N., Muntyan, A.N., Rumyantseva, T.B., and Zatovskaya, T.V., Biologicheskoe raznoobrazie kluben’kovykh bakterii v ekosistemakh i agrotsenoz. Teoreticheskie osnovy i metody (Biological Diversity of Root Nodule Bacteria in Ecosystems and Agrocenoses. Theoretical Foundations and Methods), Roumiant-seva, M.L. and Simarov B.V., Eds., S.-Pb.–Pushkin: VNIISKhM, 2011.

  37. Onishchuk, O.P., Roumiantseva, M.L., Provorov, N.A., and Simarov, B.V., Variability of Sinorhizobium meliloti strains in characteristics determining their saprophytic survival under salinization conditions, Sel’skokhoz. Biol., 2009, no. 1, pp. 77–82.

    Google Scholar 

  38. Roumiantseva, M.L., Onischuk, O.P., Belova, V.S., Kurchak, O.N., and Simarov B.V., Polymorphism of Sinorhizobium meliloti strains isolated from diversity centers of alfalfa in various soil and climatic conditions, Rus. J. Genet.: Appl. Res., 2011, vol. 1, no. 2, pp. 97–102.

    Article  Google Scholar 

  39. Alloing, G., Travers, I., and Sagot, B., Le Rudulier, D., and Dupont, L., Proline betaine uptake in Sinorhizo bium meliloti: characterization of Prb, an Opplike ABC transporter regulated by both proline betaine and salinity stress, J. Bacteriol., 2006, vol. 188, no. 17, pp. 6308–6317.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Galibert, F., Finan, T.M., Long, S.R., Puehler, A., Abola, P., Ampe, F., BarloyHubler, F., Barnett, M.J., Becker, A., Boistard, P., Bothe, G., Boutry, M., Bowser, L., Buhrmester, J., Cadieu, E., Capela, D., Chain, P., Cowie, A., Davis, R.W., Dreano, S., Federspiel, N.A., Fisher, R.F., Gloux, S., Godrie, T., Goffeau, A., Golding, B., Gouzy, J., Gurjal, M., HernandezLucas, I., Hong, A., Huizar, L., Hyman, R.W., Jones, T., Kahn, D., Kahn, M.L., Kalman, S., Keating, D.H., Kiss, E., Komp, C., Lelaure, V., Masuy, D., Palm, C., Peck, M.C., Pohl, T.M., Portetelle, D., Purnelle, B., Ramsperger, U., Surzycki, R., Thebault, P., Vandenbol, M., Vorholter, F.J., Weidner, S., Wells, D.H., Wong, K., Yeh, K.C., and Batut, J., The composite genome of the legume sym biont Sinorhizobium meliloti, Science, 2001, vol. 293, no. 5530, pp. 668–672.

    Article  CAS  PubMed  Google Scholar 

  41. Sun, S., Guo, H., and Xu, J., Multiple gene genealogi cal analyses reveal both common and distinct popula tion genetic patterns among replicons in the nitrogen fixing bacterium Sinorhizobium meliloti, Microbiology (UK), 2006, vol. 152, pp. 3245–3259.

    Article  CAS  PubMed  Google Scholar 

  42. Guo, H., Sun, S., Finan, T.M., and Xu, J., Novel DNA sequences from natural strains of the nitrogenfixing symbiotic bacterium Sinorhizobium meliloti, Appl. Environ. Microbiol., 2005, vol. 71, no. 11, pp. 7130–7138.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Schwedock, J.S. and Long, S.R., Rhizobium meliloti genes involved in sulfate activation: the two copies of nodPQ and a new locus, saa, Genetics, 1992, vol. 132, no. 4, pp. 899–909.

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Reguera, M., Lloret, J., Margaret, I., Vinardell, J.M., Martin, M., Buendia, A., Rivilla, R., RuizSainz, J.E., Bonilla, I., and Bolanos, L., Gene Smb21071 of plas mid pSymB is required for osmoadaptation of Sinorhizobium meliloti 1021 and is implicated in modi fications of cell surface polysaccharides structure in response to hyperosmotic stress, Can. J. Microbiol., 2009, vol. 10, pp. 1145–1152.

    Article  Google Scholar 

  45. Stiens, M., Schneiker, S., Keller, M., Kuhn, S., Puehler, A., and Schlueter, A., Sequence analysis of the 144kilobase accessory plasmid pSmeSM11a, isolated from a dominant Sinorhizobium meliloti strain identi fied during a longterm field release experiment, Appl. Environ. Microbiol., 2006, vol. 72, pp. 3662–3672.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Stiens, M., Schneiker, S., Puehler, A., and Schlueter, A., Sequence analysis of the 181kb accessory plasmid pSmeSM11b, isolated from a dominant Sinorhizobium meliloti strain identified during a longterm field release experiment, FEMS Microbiol. Lett., 2007, vol. 271, pp. 297–309.

    Article  CAS  PubMed  Google Scholar 

  47. Roumiantseva, M.L., Andronov, E.E., Sagulenko, V.V. Onishuk, O.P., Provorov, N.A., and Simarov, B.V., Plasmids in strain Sinorhizobium meliloti P108 in the course of symbiosis with alfalfa Medicago sativa, Russ. J. Genet., 2004, vol. 40, no. 4, pp. 356–362.

    Article  CAS  Google Scholar 

  48. Ermilova, E.V., Molekulyarnye aspekty adaptatsii prokariot (Molecular Aspects of Prokaryotic Adapta tion), St. Petersburg: Khimizdat, 2012.

    Google Scholar 

  49. McIntyre, H.J., Davies, H., Hore, T.A., Miller, S.H., Dufour, J.P., and Ronson, C.W., Trehalose biosynthesis in Rhizobium leguminosarum bv. trifolii and its role in desiccaion tolerance, Appl. Environ. Microbiol., 2007, vol. 73, no. 12, pp. 3984–3992.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. Vriezen, J.A.C., de Bruijn, F.J., and Nuesslein, K., Desiccation responses and survival of Sinorhizobium meliloti USDA 1021 in relation to growth phase, tem perature, chloride and sulfate availability, Lett. Appl. Microbiol., 2006, vol. 42, no. 2, pp. 172–178.

    Article  CAS  PubMed  Google Scholar 

  51. Becker, A., Schmidt, M., Jaeger, W., and Puehler, A., New gentamicinresistance and lacZ promoterprobe cassettes suitable for insertion mutagenesis and genera tion of transcriptional fusions, Gene, 1995, vol. 162, pp. 37–39.

    Article  CAS  PubMed  Google Scholar 

  52. Vinuesa, P., NeumannSilkow, F., PaciosBras, C., Spaink, H.P., MartinezRomero, E., and Werner, D., Genetic analysis of a pHregulated operon from Rhizo bium tropici CIAT899 involved in acid tolerance and nodulation competitiveness, Mol. Plant–Microbe Inter act., 2003, vol. 16, no. 2, pp. 159–168.

    Article  CAS  Google Scholar 

  53. Wei, W., Gu, Z.J., Zhang, B., Wang, L., and Yang, S.S., Cloning and complementation analysis of greA gene involved in salt tolerance of Sinorhizobium meliloti, Ann. Microbiol., 2007, vol. 57, no. 2, pp. 289–291.

    Article  CAS  Google Scholar 

  54. Jiang, J.Q., Wei, W., Du, B.H., Li, X.H., Wang, L., and Yang, S.S., Salttolerance genes involved in cation efflux and osmoregulation of Sinorhizobium fredii RT19 detected by isolation and characterization of Tn5 mutants, FEMS Microbiol. Lett., 2004, vol. 239, no. 1, pp. 139–146.

    Article  CAS  PubMed  Google Scholar 

  55. Chizhevskaya, E.P., Onishchuk, O.P., Andronov, E.E., and Simarov, B.V., Application of sitedirected mutagenesis for investigation of the function of the SMb20332 gene in root nodule bacteria Sinorhizobium meliloti, Sel’skokhoz. Biol., 2011, no. 3, pp. 55–61.

    Google Scholar 

  56. Belova, V.S., Yurgel’, S.N., Rais, D., Rumyantseva, T.B., Simarov, B.V., and Roumiantseva, M.L., Survival of Sinorhizobium meliloti strain CIAM1775 in soils of differ ent acidity, in Materialy Vserossiiskoi nauchnoprak ticheskoi konferentsii “Perspektivnye napravleniya issledo vanii v zemledelii i rastenievodstve” UlGTU (Proc. AllRuss. Sci.Pract. Conf. “Prospective Directions of Research in Agriculture and Crop Sector), Ul’yanovsk, 2011, pp. 35–39.

    Google Scholar 

  57. Ohwada, T., Sasaki, Y., Koike, H., Igawa, K., and Sato, T., Correlation between NaCl sensitivity of Rhizobium bacteria and ineffective nodulation of legu minous plants, Boisci. Biotechnol. Biochem., 1998, vol. 62, no. 11, pp. 2086–2090.

    Article  CAS  Google Scholar 

  58. Chien, C.T., Maundu, J., Cavaness, J., Dandurand, L.M., and Orser, C.S., Characterization of salt tolerant and saltsensitive mutants of Rhizobium legu minosarum bv. viciae strain C12046, FEMS Microbiol. Lett., 1992, vol. 90, pp. 135–140.

    Article  CAS  Google Scholar 

  59. Pobigaylo, N., Szymczak, S., Nattkemper, T.W., and Becker, A., Identification of genes relevant to symbiosis and competitiveness in Sinorhizobium meliloti using sig naturetagged mutants, Mol. Plant–Microbe Interact., 2008, vol. 21, no. 2, pp. 219–231.

    Article  CAS  PubMed  Google Scholar 

  60. Pobigaylo, N., Wetter, D., Szymczak, S., Schiller, U., Kurtz, S., Meyer, F., Nattkemper, T.W., and Becker, A., Construction of a large signaturetagged miniTn5 transposon library and its application to mutagenesis of Sinorhizobium meliloti, Appl. Environ. Microbiol., 2006, vol. 72, no. 6, pp. 4329–4337.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. GuaschVidal, B., Brussel, A.A.N., Estevez, J., Bellogin, R., Ollero, F.J., Espuny, M.R., and Megias, M., Nod factor production and abiotic stress in Rhizobium, in Beneficial PlantMicrobial Interactions. Ecology and Applications, Belen Rodelas Gonzalez, M. and Gonza lezLopez, J., Eds., New York: CRC, 2013, pp. 71–98.

  62. DominguezFerreras, A., PerezArnedo, R., Becker, A., Olivares, J., Soto, M.J., and Sanjuan, J., Transcriptome profiling reveals the importance of plasmid pSymB for osmoadaptation of Sinorhizobium meliloti, J. Bacteriol., 2006, vol. 188, pp. 7617–7626.

    Article  CAS  Google Scholar 

  63. Boscari, A., Mandon, K., Dupont, L., and Poggi, M.C., and Le Rudulier, D., BetS is a major glycine betaine/pro line betaine transporter required for early osmotic adjust ment in Sinorhizobium meliloti, J. Bacteriol., 2002, vol. 184, no. 10, pp. 2654–2663.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Angelidis, A.S. and Smith, G.M., Role of the glycine betaine and carnitine transporters in adaptation of Listeria monocytogenes to chill stress in defined medium, Appl. Environ. Microbiol., 2003, vol. 69, no. 12, pp. 7492–7498.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  65. Davidson, A.L., Dassa, E., Orelle, C., and Chen, J., Structure, function, and evolution of bacterial ATP binding cassette systems, Microbiol. Mol. Biol. Rev., 2008, vol. 72, pp. 317–364.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  66. Pumirat, P., Cuccui, J., Stabler, R.A., Stevens, J.M., Muangsombut, V., Singsuksawat, E., Stevens, M.P., Wren, B.W., and Korbsrisate, S., Global transcriptional profiling of Burkholderia pseudomallei under salt stress reveals differential effects on the Bsa type III secretion system, BMC Microbiol., 2010, vol. 14. doi: 10.1186/1471218010171

  67. Sagot, B., Gaysinski, M., Mehiri, M., Guigonis, J.M., Le Rudulier, D., and Alloing, G., Osmotically induced synthesis of the dipeptide Nacetylglutaminyl glutamine amide is mediated by a new pathway con served among bacteria, Proc. Natl. Acad. Sci. U. S. A., 2010, vol. 107, no. 28, pp. 12652–12657.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  68. Rueberg, S., Tian, Z.X., Krol, E., Linke, B., Meyer, F., Wang, Y., Puehler, A., Weidner, S., and Becker, A., Con struction and validation of a Sinorhizobium meliloti whole genome DNA microarray: genomewide profiling of osmoadaptive gene expression, J. Biotechnol., 2003, vol. 106, pp. 255–268.

    Article  Google Scholar 

  69. Finan, T.M., Weidner, S., Wong, K., Buhrmester, J., Chain, P., Vorhoelter, F.J., HernandezLucas, I., Becker, A., Cowie, A., Gouzy, J., Golding, B., and Puehler, A., The complete sequence of the 1.683kb pSymB megaplasmid from the N2fixing endosymbiont Sinorhizobium meliloti, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, no. 17, pp. 9889–9894.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  70. Muntyan, V.S. and Roumiantseva, M.L., Core genome of stressresistant Sinorhizobium spp. strains, inoculants of economically important leguminous host plants, in Materialy Mezhdunarodnoi nauchnoprakticheskoi kon ferentsii “Biotekhnologiya: i kachestvo zhizni” (Proc. Int. SciPract. Conf. “Biotechnology and Quality of Life”), Moscow, 2014, vol. 2, p. 15.

    Google Scholar 

  71. Park, H.D., Lee, D.H., Hong, Y.H., Kang, D.H., Lee, Y.K., Song, J., Lee, S.Y., Kim, J.W., Ki, C.S., and Lee, Y.W., Three Korean patients with maple syrup urine disease: four novel mutations in the BCKDHA gene, Ann. Clin. Lab. Sci., 2011, vol. 41, no. 2, pp. 167–173.

    CAS  PubMed  Google Scholar 

  72. Los’, D.A., Structure, regulation of expression, an functioning of fatty acid desaturases, Usp. Biol. Khim., 2001, vol. 41, pp. 163–198.

    Google Scholar 

  73. Aguilar, P.S. and de Mendoza, D., Control of fatty acid desaturation: a mechanism conserved from bacteria to humans, Mol. Microbiol., 2006, vol. 62, no. 6, pp. 1507–1514.

    Article  CAS  PubMed  Google Scholar 

  74. Pocard, J.A., Vincent, N., Boncompagni, E., Smith, L.T., Poggi, M.C., and Le Rudulier, D., Molecular character ization of the bet genes encoding glycine betaine synthesis in Sinorhizobium meliloti 102F34, Microbiology (UK), 1997, vol. 143, Pt 4, pp. 1369–1379.

    Article  CAS  PubMed  Google Scholar 

  75. Yurgel, S., Rice, J., Mulder, M., Kahn, M., Belova, V., and Roumiantseva, M., Truncated betB2144 plays a critical role in Sinorhizobium meliloti Rm2011 osmo protection and glycinebetaine catabolism, Eur. J. Soil Biol., 2013, vol. 54, pp. 48–55.

    Article  CAS  Google Scholar 

  76. VelascoGarcia, R., GonzalezSegura, L., and Munoz-Clares, R.A., Steadystate kinetic mechanism of the NADP+-and NAD+-dependent reaction catalyzed by betaine aldehyde dehydrogenase from Pseudomonas aeruginosa, Biochem. J., 2000, vol. 352, pp. 675–683.

    Article  CAS  Google Scholar 

  77. Cregut, M., Durand, M.J., and Thouand, G., The diversity and functions of choline sulphatases in micro organisms, Microb. Ecol., 2014, vol. 67, no. 2, pp. 350–357. doi: 10.1007/s0024801303287. Epub 2013.

    Article  CAS  PubMed  Google Scholar 

  78. MunozClares, R.A., DiazSanchez, A.G., Gonzalez-Segura, L., and Montiel, C., Kinetic and structural fea tures of betaine aldehyde dehydrogenases: mechanistic and regulatory implications, Arch. Biochem. Biophys., 2010, vol. 493, no. 1, pp. 71–81.

    Article  CAS  Google Scholar 

  79. Smith, L.T., Pocard, J.A., Bernard, T., and Le Rudulier, D., Osmotic control of glycine betaine biosynthe sis and degradation in Rhizobium meliloti, J. Bacteriol., 1988, vol. 170, no. 7, pp. 3142–3149.

    CAS  PubMed Central  PubMed  Google Scholar 

  80. Canovas, D., Vargas, C., Kneip, S., Moron, M.J., Ventosa, A., Bremer, E., and Nieto, J.J., Characterization of the genes for the synthesis of the compatible solute glycine betaine in the moderately halophilic bacterium Halomonas elongate DSM 3043, Microbiology (UK), 2000, vol. 146, pp. 455–463.

    CAS  PubMed  Google Scholar 

  81. Vargas, C., Argandona, M., ReinaBueno, M., RodriguezMoya, J., FernandezAunion, C., and Nieto, J.J., Unravelling the adaptation responses to osmotic and temperature stress in Chromohalobacter salexigens, a bac terium with broad salinity tolerance, Saline Systems, 2008, vol. 4, no. 14. doi:10.1186/17461448414

    Google Scholar 

  82. Mandon, K., Osteras, M., Boncompagni, E., Trinchant, J.C., Spennato, G., Poggi, M.C., and Le Rudulier, D., The Sinorhizobium meliloti glycine betaine biosynthetic genes (betlCBA) are induced by choline and highly expressed in bacteroids, Mol. Plant–Microbe Interact., 2003, vol. 16, no. 8, pp. 709–719.

    Article  CAS  PubMed  Google Scholar 

  83. Lamark, T., Rokenes, T.P., McDougall, J., and Strom, A.R., The complex bet promoters of Escheri chia coli: regulation by oxygen (ArcA), choline (BetI), and osmotic stress, J. Bacteriol., 1996, vol. 178, no. 6, pp. 1655–1662.

    CAS  PubMed Central  PubMed  Google Scholar 

  84. Ziegler, C., Bremer, E., and Kraemer, R., The BCCT family of carriers: from physiology to crystal structure, Mol. Microbiol., 2010, vol. 78, no. 1, pp. 13–34.

    CAS  PubMed  Google Scholar 

  85. Wyn-Jones, R.G. and Storey, R., Betaines, in The Phys iology and Biochemistry of Drought Resistance in Plant, Paleg, I.G. and Aspinall, D., Eds., Sydney: Academic, 1981, pp. 117–204.

  86. Osteras, M., Boncompagni, E., Vincent, N., Poggi, M.C., and Le Rudulier, D., Presence of a gene encoding choline sulfatase in Sinorhizobium meliloti bet operon: cholineO sulfate is metabolized into glycine betaine, Proc. Natl. Acad. Sci. U. S. A., 1998, vol. 95, pp. 11394–11399.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  87. Selye, H.A., Syndrome produced by diverse nocuos agents, Nature, 1936, vol. 138, p. 32

    Article  Google Scholar 

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  1. All-Russia Research Institute for Agricultural Microbiology, St. Petersburg-Pushkin, Russia

    M. L. Roumiantseva & V. S. Muntyan

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  1. M. L. Roumiantseva
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Original Russian Text © M.L. Roumiantseva, V.S. Muntyan, 2015, published in Mikrobiologiya, 2015, Vol. 84, No. 3, pp. 263–280.

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Roumiantseva, M.L., Muntyan, V.S. Root nodule bacteria Sinorhizobium meliloti: Tolerance to salinity and bacterial genetic determinants. Microbiology 84, 303–318 (2015). https://doi.org/10.1134/S0026261715030170

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