An overview of the metabolic differences between Bradyrhizobium japonicum 110 bacteria and differentiated bacteroids from soybean (Glycine max) root nodules: An in vitro 13C- and 31P-nuclear magnetic resonance spectroscopy study

FEMS Microbiology Letters

Volumn 343, Issue 1, 2013, Pages 49-56

  Vauclare, Pierre ^a,b   Bligny, Richard ^c   Gout, Elisabeth ^c   Widmer, François ^a  

^a Biologie Moléculaire Végétale   (Switzerland)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^c CEA GRENOBLE   (France)

Author keywords

Bradyrhizobium japonicum; Metabolism; NMR

Indexed keywords

CARBOHYDRATE; GLUTAMIC ACID; HOMOSPERMIDINE; INOSITOL; NUCLEOTIDE; TREHALOSE; UNCLASSIFIED DRUG;

ADAPTATION; BACTERIAL CELL; BACTERIAL METABOLISM; BACTERIUM; BACTERIUM ISOLATION; BACTEROID; BIOACCUMULATION; BRADYRHIZOBIUM JAPONICUM; CARBON METABOLISM; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; HOST; IN VITRO STUDY; LETTER; METABOLITE; MICROENVIRONMENT; NITROGEN FIXATION; NODULATION; NONHUMAN; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PLANT CELL; PRIORITY JOURNAL; RHIZOBIACEAE; SOIL MICROFLORA; SOYBEAN;

BRADYRHIZOBIUM; CARBOHYDRATES; MAGNETIC RESONANCE SPECTROSCOPY; METABOLOME; NUCLEOTIDES; PHOSPHATES; ROOT NODULES, PLANT; SOYBEANS;

BRADYRHIZOBIUM JAPONICUM; GLYCINE MAX;

EID: 84877620314     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/1574-6968.12124     Document Type: Letter

References (48)

1. Abe H (1994) Polyamines in leguminous nodules with special reference to homospermidine synthesis. PhD Thesis, University of Tsukuba, Ibaraki, Japan.
2. Boscari A, Van de Sype G, Le Rudulier D & Mandon K (2006) Overexpression of BetS, a Sinorhizobium meliloti high-affinity betaine transporter, in bacteroids from Medicago sativa nodules sustains nitrogen fixation during early salt stress adaptation. Mol Plant Microbe Interact 19: 896-903.
3. Boutte CC, Srinivasan BS, Flannick JA, Novak AF, Martens AT, Batzoglou S, Viollier PH & Crosson S (2008) Genetic and computational identification of a conserved bacterial metabolic module. PLoS Genet 4: 1-12.
4. Brechenmacher L, Lei Z, Libault M, Findley S, Sugawara M, Sadowsky MJ, Sumner LW & Stacey G (2010) Soybean metabolites regulated in root hairs in response to the symbiotic bacterium Bradyrhizobium japonicum. Plant Physiol 153: 1808-1822.
5. Brewin NJ (2004) Cell wall remodelling in the Rhizobium-legume symbiosis. Crit Rev Plant Sci 23: 1-24.
6. Chattopadhyay MK, Tabor CW & Tabor H (2003) Polyamines protect Escherichia coli cells from the toxic effect of oxygen. P Natl Acad Sci USA 100: 2261-2265.
7. Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103: 1355-1365.
8. Dean RM, Rivers RL, Zeidel ML & Roberts DM (1999) Purification and functional reconstitution of soybean nodulin 26. An aquaporin with water and glycerol transport properties. Biochemistry 38: 347-353.
9. Delmotte N, Ahrens CH, Knief C, Qeli E, Koch M, Fischer HM, Vorholt JA, Hennecke H & Pessi G (2010) An integrated proteomics and transcriptomics reference data set provides new insights into the Bradyrhizobium japonicum bacteroid metabolism in soybean root nodules. Proteomics 10: 1391-1400.
10. Fougère F & Le Rudulier D (1990) Uptake of glycine betaine and its analogues by bacteroids of Rhizobium meliloti. J Gen Microbiol 136: 157-163.
11. Fujihara S (2009) Biogenic amines in rhizobia and legume root nodules. Microbes Environ 24: 1-13.
12. 2+, glutamate and homospermidine. Microbiology 140: 1909-1916.
13. Fujihara S, Abe H, Minagawa Y, Akao S & Yoneyama T (1994) Polyamines in nodules from various plant-microbe symbiotic associations. Plant Cell Physiol 35: 1127-1134.
14. Gout E, Aubert S, Bligny R, Rébeillé F, Nonomura AR, Benson AA & Douce R (2000) Metabolism of methanol in plant cells. Carbon-13 nuclear magnetic resonance studies. Plant Physiol 123: 287-296.
15. Green LS & Emerich DW (1997) Bradyrhizobium japonicum does not require α-ketoglutarate dehydrogenase for growth on succinate or malate. J Bacteriol 179: 194-201.
16. Hoelzle I & Streeter JG (1990) Increased accumulation of trehalose in Rhizobia cultured under 1% oxygen. Appl Environ Microbiol 56: 3213-3215.
17. Hunt S & Layzell DB (1993) Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu Rev Plant Physiol Plant Mol Biol 44: 483-511.
18. Jiang G, Krishnan AH, Kim Y-W, Wacek TJ & Krishnan HB (2001) A functional myo-inositol dehydrogenase gene is required for efficient nitrogen fixation and competitiveness of Sinorhizobium fredii USDA191 to nodulate soybean (Glycine max [L.] Merr.). J Bacteriol 183: 2595-2604.
19. Lin J, Walsh KB, Canvin DT & Layzell DB (1988) Structural and physiological bases for effectivity of soybean nodules formed by fast-growing and slow-growing bacteria. Can J Bot 66: 526-534.
20. Mandon K, Osterås M, Boncompagni E, Trinchant JC, Spennato G, Poggi MC & Le Rudulier D (2003) The Sinorhizobium meliloti glycine betaine biosynthetic genes (betlCBA) are induced by choline and highly expressed in bacteroids. Mol Plant-Microbe Interact 16: 709-719.
21. Minder AC, de Rudder KE, Narberhaus F, Fischer HM, Hennecke H & Geiger O (2001) Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant. Mol Microbiol 39: 1186-1198.
22. Oke V & Long SR (1999) Bacteroid formation in the Rhizobium-legume symbiosis. Curr Opin Microbiol 2: 641-646.
23. Patriarca EJ, Tatè R & Iaccarino M (2002) Key role of bacterial NH(4)(+) metabolism in Rhizobium-plant symbiosis. Microbiol Mol Biol Rev 66: 203-222.
24. Patton JL, Pessoa-Brandao L & Henry SA (1995) Production and reutilization of an extracellular phosphatidylinositol catabolite, glycerophosphoinositol, by Saccharomyces cerevisiae. J Bacteriol 177: 3379-3385.
25. Perret X, Staehelin C & Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64: 180-201.
26. Pessi G, Ahrens CH, Rehrauer H, Lindemann A, Hauser F, Fischer HM & Hennecke H (2007) Genome-wide transcript analysis of Bradyrhizobium japonicum bacteroids in soybean root nodules. Mol Plant Microbe Interact 20: 1353-1363.
27. Pfeffer PE, Bécard G, Rolin DB, Uknalis J, Cooke P & Tu SI (1994) In vivo nuclear magnetic resonance study of the osmoregulation of phosphocholine-substituted beta-1, 3;1, 6 cyclic glucan and its associated carbon metabolism in Bradyrhizobium japonicum USDA 110. Appl Environ Microbiol 60: 2137-2146.
28. Prell J & Poole P (2006) Metabolic changes in rhizobia. Trends Microbiol 141: 161-168.
29. Ratcliffe HD, Drozd JW & Bull AT (1983) Growth energetics of Rhizobium leguminosarum in chemostat culture. J Gen Microbiol 129: 1697-1706.
30. Regensburger B & Hennecke H (1983) RNA polymerase from Rhizobium japonicum. Arch Microbiol 135: 103-109.
31. Reibach PH, Mask PL & Streeter JG (1981) A rapid one-step method for the isolation of bacteroids from root nodules of soybean plants, utilizing self-generating Percoll gradients. Can J Microbiol 27: 491-495.
32. Rolin DB, Pfeffer PE, Osman SF, Szwergold BS, Kappler F & Benesi AJ (1992) Structural studies of a phosphocholine substituted beta-(1, 3);(1, 6) macrocyclic glucan from Bradyrhizobium japonicum USDA 110. Biochim Biophys Acta 1116: 215-225.
33. Salminen SO & Streeter JG (1987) Involvement of glutamate in the respiratory metabolism of Bradyrhizobium japonicum bacteroids. J Bacteriol 169: 495-499.
34. Salminen SO & Streeter JG (1990) Factors contributing to the accumulation of glutamate in B. japonicum bacteroids under microaerobic conditions. J Gen Microbiol 136: 2119-2126.
35. Sarma AD & Emerich DW (2005) Global protein expression pattern of Bradyrhizobium japonicum bacteroids: a prelude to functional proteomics. Proteomics 5: 4170-4184.
36. Sarma AD & Emerich DW (2006) A comparative proteomic evaluation of culture grown vs nodule isolated Bradyrhizobium japonicum. Proteomics 6: 3008-3028.
37. Streeter JG (1985) Accumulation of α, α-trehalose by rhizobium bacteria and bacteroids. J Bacteriol 164: 78-84.
38. Streeter JD & Gomez ML (2006) Three enzyme for trehalose synthesis in Bradyrhizobium cultures bacteria and in bacteroids from soybean nodules. Appl Environ Microbiol 72: 4250-4255.
39. 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: 1071-1081.
40. Tajima S & Kouzai K (1989) Nucleotide pools in soybean nodule tissues, a survey of NAD(P)/NAD(P)H ratios and energy charge. Plant Cell Physiol 30: 589-593.
41. Tang Y & Hollingsworth RI (1998) Regulation of lipid synthesis in Bradyrhizobium japonicum: low oxygen concentration trigger phosphatidylinositol biosynthesis. Appl Environ Microbiol 64: 1963-1966.
42. Tsukada S, Aono T, Akiba N, Lee KB, Liu CT, Toyazaki H & Oyaizu H (2009) Comparative genome-wide transcriptional profiling of Azorhizobium caulinodans ORS571 grown under free-living and symbiotic conditions. Appl Environ Microbiol 75: 5037-5046.
43. Udvardi MK & Day DA (1997) Metabolite transport across symbiotic membranes of legume nodules. Annu Rev Plant Physiol Plant Mol Biol 48: 493-523.
44. Van der Rest B, Boisson A-M, Gout E, Bligny R & Douce R (2002) Glycerophosphocholine metabolism in higher plant cells. Evidence of a new glyceryl-phosphodiester phosphodiesterase. Plant Physiol 130: 244-255.
45. 13C nuclear magnetic resonance study. Planta 231: 1495-1504.
46. Whitehead LF & Day DA (1997) The peribacteroid membrane. Physiol Plant 100: 30-44.
47. Young JPW & Haukka KE (1996) Diversity and phylogeny of rhizobia. New Phytol 133: 87-94.
48. Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63: 968-989.