Symbiosis

, Volume 67, Issue 1–3, pp 103–111 | Cite as

Increased trehalose biosynthesis improves Mesorhizobium ciceri growth and symbiosis establishment in saline conditions

  • Salwa Moussaid
  • Ana Domínguez-Ferreras
  • Socorro Muñoz
  • Jamal Aurag
  • El Bekkay Berraho
  • Juan Sanjuán
Article

Abstract

Cicer arietinum (chickpea) is a legume very sensitive to salinity, and so are most of its rhizobial symbionts belonging to the species Mesorhizobium ciceri. We observed that exogenous trehalose (i.e., added to the growth medium) can significantly improve growth of M. ciceri strain Rch125 under moderate salinity. In order to test if endogenous trehalose (i.e., synthesized by the cell) could also enhance salt tolerance, strain Rch125 was genetically modified with various trehalose biosynthesis genes from Sinorhizobium meliloti 1021 (otsA, treS, treY) and Mesorhizobium loti MAFF 303099 (otsAB). We found that overexpression of otsA or otsAB, but not treS or treY, significantly improved M. ciceri Rch125 growth in saline media. This growth improvement correlated with enhanced trehalose accumulation in otsA- and otsAB-modified cells, suggesting that increased trehalose synthesis via trehalose-6-phosphate can enhance bacterial salt tolerance. Chickpea plants inoculated with M. ciceri Rch125 derivatives carrying extra otsAB or otsA genes formed more nodules and accumulated more shoot biomass than wild type inoculated plants when grown in the presence of NaCl. These results support the notion that improved salt tolerance of the bacterial symbiont can alleviate the negative effects of salinity on chickpeas, and that such improvement in M. ciceri can be achieved by manipulating trehalose metabolism.

Keywords

Stress tolerance Mesorhizobium ciceri Trehalose Osmoprotectant Symbiosis 

References

  1. Avonce N, Mendoza-Vargas A, Morett E, Iturriaga G (2006) Insights on the evolution of trehalose biosynthesis. BMC Evol Biol 6:109. doi:10.1186/1471-2148-6-109 PubMedCentralCrossRefPubMedGoogle Scholar
  2. Babber S, Sheokand S, Malik S (2000) Nodule structure and functioning in chickpea (Cicer arietinum) as affected by salt stress. Biol Plant 43:269–273CrossRefGoogle Scholar
  3. Beringer JE (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84:188–198PubMedGoogle Scholar
  4. Bianco C, Defez R (2012) Soil bacteria support and protect plants against abiotic stresses. In: A Shanker, B Venkateswarlu (eds) Abiotic stress in plants-mechanisms and adaptations doi:10.5772/23310
  5. Blatny JM, Brautaset T, Winther-Larsen HC, Haugan K, Valla S (1997) Construction and use of a versatile set of broad-host-range cloning and expression vectors based on the RK2 replicon. Appl Environ Microbiol 63:370–379PubMedCentralPubMedGoogle Scholar
  6. Bordeleau LM, Prevost D (1994) Nodulation and nitrogen fixation in extreme environments. Plant Soil 161:115–125CrossRefGoogle Scholar
  7. Cardoso FS, Castro RF, Borges N, Santos H (2007) Biochemical and genetic characterization of the pathways for trehalose metabolism in Propionibacterium freudenreichii, and their role in stress response. Microbiology 153:270–280CrossRefPubMedGoogle Scholar
  8. Carpinelli J, Krämer R, Agosin E (2006) Metabolic engineering of Corynebacterium glutamicum for trehalose overproduction: Role of the TreYZ trehalose biosynthetic pathway. Appl Environ Microbiol 72:1949–1955PubMedCentralCrossRefPubMedGoogle Scholar
  9. Crowe JH (2007) Trehalose as a chemical chaperone fact and fantasy. Adv Exp Med Biol 594:143–158CrossRefPubMedGoogle Scholar
  10. Csonka LN (1989) Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev 53:121–147PubMedCentralPubMedGoogle Scholar
  11. De Smet KA, Wetson A, Brown IN, Young DB, Robertson BD (2000) Three pathways for trehalose biosynthesis in mycobacteria. Microbiology 146:199–208CrossRefPubMedGoogle Scholar
  12. Dominguez-Ferreras A, Perez-Arnedo R, Becker A, Olivares J, Soto MJ, Sanjuan J (2006) Transcriptome profiling reveals the importance of plasmid pSmbB for osmoadaptation of Sinorhizobium meliloti. J Bacteriol 188:7617–7625PubMedCentralCrossRefPubMedGoogle Scholar
  13. Domínguez-Ferreras A, Soto MJ, Pérez-Arnedo R, Olivares J, Sanjuán J (2009) Importance of trehalose biosynthesis for Sinorhizobium meliloti osmotolerance and nodulation of alfalfa roots. J Bacteriol 191(24):7490–7499PubMedCentralCrossRefPubMedGoogle Scholar
  14. Eis C, Watkins M, Prohaska T, Nidetzky B (2001) Fungal trehalose phosphorylase: kinetic mechanism, pH-dependence of the reaction and some structural properties of the enzyme from Schizophyllum commune. Biochem J 356:757–767PubMedCentralCrossRefPubMedGoogle Scholar
  15. Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27RCrossRefPubMedGoogle Scholar
  16. Farias-Rodriguez R, Mellor RB, Arias C, Pena-Cabriales JJ (1998) The accumulation of trehalose in nodules of several cultivars of common bean (Phaseolus vulgaris) and its correlation with resistance to drought stress. Plant Physiol 102:353–359CrossRefGoogle Scholar
  17. Flowers TJ, Gaur PM, Gowda CL, Krishnamurthy L, Samineni S, Siddique KH, Turner NC, Vadez V, Varshney RK, Colmer TD (2010) Salt sensitivity in chickpea. Plant Cell Environ 33:490–509CrossRefPubMedGoogle Scholar
  18. Freeman BC, Chen C, Beattie GA (2010) Identification of the trehalose biosynthetic loci of Pseudomonas syringae and their contribution to fitness in the phyllosphere. Environ Microbiol 12:1486–1497PubMedGoogle Scholar
  19. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39CrossRefPubMedGoogle Scholar
  20. Gouffi K, Blanco C (2000) Is the accumulation of osmoprotectant the unique mechanism involved in bacterial osmoprotection. Int J Food Microbiol 55:171–174CrossRefPubMedGoogle Scholar
  21. Gouffi K, Pica N, PichereauV BC (1999) Disaccharides as new class of non accumulating osmoprotectants for Sinorhizobium meliloti. Appl Environ Microbiol 65:1491–1500PubMedCentralPubMedGoogle Scholar
  22. Han SE, Kwon HB, Lee SB, Yi BY, Murayama I, Kitamoto Y, Byun MO (2003) Cloning and characterization of a gene encoding trehalose phosphorylase (TP) from Pleurotus sajor-caju. Sci Dir 30:194–202Google Scholar
  23. Higo A, Katoh H, Ohmori K, Ikeuchi M, Ohmori M (2006) The role of a gene cluster for trehalose metabolism in dehydration tolerance of the filamentous cyanobacterium Anabaena sp. PCC 7120. Microbiology 152(14):979–987CrossRefPubMedGoogle Scholar
  24. Iturriaga G, Suárez R, Nova-Franco B (2009) Trehalose metabolism: from osmoprotection to signaling. Int J Mol Sci 10:3793–3810PubMedCentralCrossRefPubMedGoogle Scholar
  25. Kaneko T, Nakamaura Y, Sato S, Asamizu E, KatoT SS, Watanabe A, Idesawa K, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Mochizuki Y, Nakayama S, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7:331–338CrossRefPubMedGoogle Scholar
  26. Klähn S, Hagemann M (2011) Compatible solute biosynthesis in cyanobacteria. Environ Microbiol 13:551–562CrossRefPubMedGoogle Scholar
  27. Krouma A (2009) Physiological and nutritional response of chickpea (Cicer arietinum L.) to salinity. Turk J Agric For 33:503–512Google Scholar
  28. Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M (2014) Trehalose metabolism in plants. Plant J 79:544–567CrossRefPubMedGoogle Scholar
  29. Maatallah J, Berraho EB, Muñoz S, Sanjuan J, Lluch C (2002) Phenotypic and molecular characterization of chickpea rhizobia isolated from different areas of Morocco. J Appl Microbiol 93:531–540CrossRefPubMedGoogle Scholar
  30. Mc Intyre HJ, Davies H, Hore TA, Miller SH, Dufour JP, Ronson CW (2007) Trehalose biosynthesis in Rhizobium leguminosarum bv. trifolii and its role in desiccation tolerance. Appl Environ Microbiol 73:3984–3992CrossRefGoogle Scholar
  31. Meade HM, Long SR, Ruvkun GB, Brown SE, Ausubel FM (1982) Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposan Tn5 mutagenesis. J Bacteriol 149:114–122PubMedCentralPubMedGoogle Scholar
  32. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, CHS, Nueva YorkGoogle Scholar
  33. Miller KJ, Wood JM (1996) Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol 50:101–136CrossRefPubMedGoogle Scholar
  34. Müller J, Xie ZP, Staehelin C, Mellor RB, Boller T, Wiemken A (1994) Trehalose and trehalase in root nodules from various legumes. Physiol Plant 90:86–92CrossRefGoogle Scholar
  35. Nakada T, Maruta K, Mitsuzumi H, Kubota M, Chaen H, Sugimono T, Kurimoto M, Tsujisaka Y (1995) Purification and characterization of a novel enzyme, maltooligosyl trehalose trehalohydrolase, from Arthrobacter sp. Q36. Biosci Biotechnol Biochem 59:2215–2218CrossRefPubMedGoogle Scholar
  36. Nakada T, Ikegami S, Chaen H, Kubota M, Fukuda S, Sugimoto T, Kurimoto M, Tsujisaka Y (1996) Purification and characterization of thermostable maltooligosyl trehalose trehalohydrolase from the thermoacidohilic archaebacterium Sulfolobus acidocaldarius. Biosci Biotechnol Biochem 60:267–270CrossRefPubMedGoogle Scholar
  37. Nandasena KG, O’Hara GW, Tiwari RP, Willlems A, Howieson JG (2007) Mesorhizobium ciceri biovar biserrulae, a novel biovar nodulating the pasture legume Biserrula pelecinus L. Int J Syst Evol Microbiol 57:1041–1045CrossRefPubMedGoogle Scholar
  38. Nandasena KG, Yates R, Tiwari R, O’Hara G, Howieson J, Ninawi M, Chertkov O, Detter C, Tapia R, Han S, Woyke T, Pitluck S, Nolan M, Land M, Liolios K, Pati A, Copeland A, Kyrpides NC, Ivanova N, Goodwin L, Meenakshi U, Reeve W (2013) Complete genome sequence of Mesorhizobium ciceri bv. biserrulae type strain (WSM1271T). Stand Genomic Sci 9:462–472PubMedCentralCrossRefPubMedGoogle Scholar
  39. Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59(1):417–441CrossRefPubMedGoogle Scholar
  40. Pichereau V, Hartke A, Auffray Y (2000) Starvation and osmotic stress induced multiresistances. Influence of extracellular compounds. Int J Food Microbiol 55:19–25CrossRefPubMedGoogle Scholar
  41. Purvis JE, Yomano LP, Ingram LO (2005) Enhanced trehalose production improves growth of Escherichia coli under osmotic stress. Appl Environ Microbiol 71:3761–3769PubMedCentralCrossRefPubMedGoogle Scholar
  42. Reina-Bueno M, Argandoña M, Nieto JJ, Hidalgo-García A, Iglesias-Guerra F, Delgado MJ, Vargas C (2012) Role of trehalose in heat and desiccation tolerance in the soil bacterium Rhizobium etli. BMC Microbiol 12:207. doi:10.1186/1471-2180-12-207 PubMedCentralCrossRefPubMedGoogle Scholar
  43. Ruhal R, Kataria R, Choudhury B (2013) Trends in bacterial trehalose metabolism and significant nodes of metabolic pathway in the direction of trehalose accumulation. Microb Biotechnol 6(5):493–502PubMedCentralCrossRefPubMedGoogle Scholar
  44. Schiraldi C, Di Lernia I, De Rosa M (2002) Trehalose production: exploiting novel approaches. Trends Biotechnol 20:420–425CrossRefPubMedGoogle Scholar
  45. Schluepmann H, Berke L, Sanchez-Perez GF (2012) Metabolism control over growth: a case for trehalose-6-phosphate in plants. J Exp Bot 63:3379–3390CrossRefPubMedGoogle Scholar
  46. Simon R, Priefer U, Pûhler A (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotech 1:784–791CrossRefGoogle Scholar
  47. Soussi M, Ocana A, Lluch C (1998) Effects of salt stress on growth, photosynthesis and nitrogen fixation in chickpea (Cicer aritiunum). J Exp Bot 49:1329–1337CrossRefGoogle Scholar
  48. Streeter JG (1985) Accumulation of α, α -trehalose by rhizobium bacteria and bacteroids. J Bacteriol 164:78–84PubMedCentralPubMedGoogle Scholar
  49. Streeter JG, Bhagwat A (1999) Biosynthesis of trehalose from maltooligosaccharides in rhizobia. Can J Microbiol 45:716–721CrossRefPubMedGoogle Scholar
  50. Suárez R, Wong A, Ramírez M, Barraza A, Orozco MC, Cevallos MA, Lara M, Hernández G, Iturriaga G (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6 phosphate synthase in rhizobia. Mol Plant Microbe Interact 21:958–966CrossRefPubMedGoogle Scholar
  51. Sugawara M, Cytryn EJ, Sadowsky MJ (2010) Functional role of Bradyrhizobium japonicum trehalose biosynthesis and metabolism genes during physiological stress and nodulation. Appl Environ Microbiol 76(4):1071–1081PubMedCentralCrossRefPubMedGoogle Scholar
  52. Tejera NA, Iribarne C, Lopez M, Herrera-Cervera JA, Lluch C (2005) Physiological implications of trehalose from Phaseolus vulgaris root nodules: partial purification and characterization. Plant Physiol Biochem 43:355–361CrossRefGoogle Scholar
  53. Vincent JM (1970) A Manual for the Practical Study of Root-Nodule Bacteria. Oxford, England 164pGoogle Scholar
  54. Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Salwa Moussaid
    • 1
  • Ana Domínguez-Ferreras
    • 2
  • Socorro Muñoz
    • 2
  • Jamal Aurag
    • 1
  • El Bekkay Berraho
    • 1
  • Juan Sanjuán
    • 2
  1. 1.Laboratory of Microbiology and Molecular Biology, Faculty of SciencesUniversity Mohammed VRabatMorocco
  2. 2.Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, CSICGranadaSpain

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