DOI QR코드

DOI QR Code

Nitrate Uptake in the Halotolerant Cyanobacterium Aphanothece halophytica is energy-dependent driven by ΔpH

  • Incharoensakdi, Aran (Department of Biochemistry and Program of Biotechnology, Faculty of Science, Chulalongkorn University) ;
  • Laloknam, Surasak (Department of Biochemistry and Program of Biotechnology, Faculty of Science, Chulalongkorn University)
  • 발행 : 2005.07.31

초록

The energetics of nitrate uptake by intact cells of the halotolerant cyanobacterium Aphanothece halophytica were investigated. Nitrate uptake was inhibited by various protonophores suggesting the coupling of nitrate uptake to the proton motive force. An artificially-generated pH gradient across the membrane (${\Delta}pH$) caused an increase of nitrate uptake. In contrast, the suppression of ${\Delta}pH$ resulted in a decrease of nitrate uptake. The increase of external pH also resulted in an enhancement of nitrate uptake. The generation of the electrical potential across the membrane ($\Delta\psi$) resulted in no elevation of the rate of nitrate uptake. On the other hand, the valinomycin-mediated dissipation of $\Delta\psi$ caused no depression of the rate of nitrate uptake. Thus, it is unlikely that $\Delta\psi$ participated in the energization of the uptake of nitrate. However, $Na^+$-gradient across the membrane was suggested to play a role in nitrate uptake since monensin which collapses $Na^+$-gradient strongly inhibited nitrate uptake. Exogenously added glucose and lactate stimulated nitrate uptake in the starved cells. N, N'-dicyclohexylcarbodiimide, an inhibitor of ATPase, could also inhibit nitrate uptake suggesting that ATP hydrolysis was required for nitrate uptake. All these results indicate that nitrate uptake in A. halophytica is ATP-dependent, driven by ${\Delta}pH$ and $Na^+$-gradient.

키워드

참고문헌

  1. Allende, J. L., Gibello, A., Fortun, A., Mengs, G., Ferrer, E. and Martin, M. (2000) 4-Hydroxybenzoate uptake in an isolated soil Acinetobacter sp. Curr. Microbiol. 40, 34-39 https://doi.org/10.1007/s002849910007
  2. Allende, J. L., Gibello, A., Fortun, A., Sanchez, M. and Martin, M. (2002) 4-Hydroxybenzoate uptake in Klebsiella planticola strain DSZ1 is driven by ${\Delta}pH$. Curr. Microbiol. 44, 31-37 https://doi.org/10.1007/s00284-001-0070-0
  3. Booth, I. R. (1985) Regulation of cytoplasmic pH in bacteria. Microbiol. Rev. 49, 359-378
  4. Crawford, N. M. and Glass, A. D. M. (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci. 3, 389-395 https://doi.org/10.1016/S1360-1385(98)01311-9
  5. Ekiel, I., Jarrel, K. F. and Sprot, G. D. (1985) Amino acid biosynthesis and sodium-dependent transport in Methanococcus voltae, as revealed by $^13$C-NMR. Eur. J. Biochem. 149, 437-444 https://doi.org/10.1111/j.1432-1033.1985.tb08944.x
  6. Espie, G. S. and Kandasamy, R. A. (1994) Monensin inhibition of $Na^+$-dependent $HCO_3$- transport distinguishes it from $Na^+$-independent transport and provides evidence for $Na^+$-/$HCO_3$- symport in the cyanobacterium Synechococcus UTEX 625. Plant Physiol. 104, 1419-1428
  7. Flores, E. and Herrero, A. (1994) Assimilatory nitrogen metabolism and its regulation; in The Molecular Biology of Cyanobacteria, Bryant, D. A. (ed.), pp. 487-517, Kluwer Academic Publishers, Dordrecht, the Netherland
  8. Garcia-Sanchez, M. J., Jaime, M. P., Ramos, A., Sanders, D. and Fernandez, J. A. (2000) Sodium-dependent nitrate transport at the plasma membrane of leaf cells of the marine higher plant Zostera marina L. Plant Physiol. 122, 879-885 https://doi.org/10.1104/pp.122.3.879
  9. Incharoensakdi, A. and Waditee, R. (2000) Degradation of glycine betaine by betaine-homocysteine methyltransferase in Aphanothece halophytica: effect of salt downshock and starvation. Curr. Microbiol. 41, 227-231 https://doi.org/10.1007/s002840010125
  10. Incharoensakdi, A. and Wangsupa, J. (2003) Nitrate uptake by the halotolerant cyanobacterium Aphanothece halophytica grown under non-stress and salt-stress conditions. Curr. Microbiol. 47, 255-259 https://doi.org/10.1007/s00284-002-4000-6
  11. Incharoensakdi, A. and Wutipraditkul, N. (1999) Accumulation of glycine betaine and its synthesis from radioactive precursors under salt-stress in the cyanobacterium Aphanothece halophytica. J. Appl. Phycol. 11, 515-523 https://doi.org/10.1023/A:1008186309006
  12. Joshi, A. K., Ahmed, S. and Ferro-Luzzi, G. (1989) Energy coupling in bacterial periplasmic transport systems. J. Biol. Chem. 264, 2126-2133
  13. Kroll, R. G. and Booth, I. R. (1981) The role of potassium transport in the generation of a pH gradient in Escherichia coli. Biochem. J. 198, 691-698
  14. Krulwich, T. A. and Guffanti, A. A. (1989) The Na+cycle of extreme alkalophiles: a secondary $Na^+$/$H^+$ antiporter and $Na^+$/solute symporters. J. Bioenerg. Biomembr. 21, 663-677 https://doi.org/10.1007/BF00762685
  15. Lara, C., Romero, J. M. and Guerrero, M. G. (1987) Regulated nitrate transport in the cyanobacterium Anacystis nidulans. J. Bacteriol. 169, 4376-4378.
  16. Mackinney, G. (1941) Absorption of light by chlorophyll solutions. J. Biol. Chem. 140, 314-322
  17. Meharg, A. A. and Blatt, M. R. (1995) $NO_3$ - transport across the plasma membrane of Arabidopsis thaliana root hairs: kinetic control by pH and membrane voltage. J. Membr. Biol. 145, 49-66 https://doi.org/10.1007/BF00233306
  18. Miller, A. J. and Smith, S. J. (1996) Nitrate transport and compartmentation in cereal root cells. J. Exp. Bot. 47, 843-854 https://doi.org/10.1093/jxb/47.7.843
  19. Mochizuki-Oda, N. and Oosawa, F. (1985) Amiloride-sensitive $Na^+$-$H^+$ antiporter in Escherichia coli. J. Bacteriol. 163, 395-397
  20. Molenaar, D., Hagting, A., Alkema, H., Driessen, A. J. M. and Konings, W. N. (1993) Characteristics and osmoregulatory roles of uptake systems for proline and glycine betaine in Lactococcus lactis. J. Bacteriol. 175, 5438-5444
  21. Omata, T. (1995) Structure, function and regulation of the nitrate transport system of the cyanobacterium Synechococcus sp. PCC 7942. Plant Cell Physiol. 36, 207-213
  22. Padan, E. and Schuldiner, S. (1996) Bacterial $Na^+$/$H^+$antiporters: molecular biology, biochemistry, and physiology; in Handbook of Biological Physics, Konings, W. N., Kaback, H. R. and Lolkema, J. S. (eds.), pp. 501-531, Elsevier Science, Amsterdam, the Netherlands
  23. Padan, E. and Schuldiner, S. (1978) Energy transduction in the photosynthetic membranes of the cyanobacterium Plectonema boryanum. J. Biol. Chem. 253, 3281-3286
  24. Pressman, B. C. (1976) Biological application of ionophores. Annu. Rev. Biochem. 45, 501-530 https://doi.org/10.1146/annurev.bi.45.070176.002441
  25. Proctor, L. M., Lai, R. and Gunsalus, R. P. (1997) The methanogenic archaeon Methanosarcina thermophila TM-1 possesses a high affinity glycine betaine transporter involved in osmotic adaptation. Appl. Environ. Microbiol. 63, 2252-2257
  26. Reed, P. W. (1979) Ionophores. Meth, Enzymol. 55, 435-454. https://doi.org/10.1016/0076-6879(79)55058-7
  27. Rodriguez, R., Guerrero, M. G. and Lara, C. (1994) Mechanism of sodium/ nitrate symport in Anacystis nidulans R2. Biochim. Biophys. Acta. 1187, 250-254 https://doi.org/10.1016/0005-2728(94)90121-X
  28. Rodriguez, R., Lara, C. and Guerrero, M. G. (1992) Nitrate transport in the cyanobacterium Anacystis nidulans R2: kinetic and energetic aspects. Biochem. J. 282, 639-643
  29. Takabe, T., Incharoensakdi, A., Arakawa, K. and Yokota, S. (1988) $CO_2$ fixation and RuBisCO content increase in a highly halotolerant cyanobacterium Aphanothece halophytica, grown in high salinity. Plant Physiol. 88, 1120-1124 https://doi.org/10.1104/pp.88.4.1120
  30. Waditee, R., Hibino, T., Nakamura, T., Incharoensakdi, A. and Takabe, T. (2002) Overexpression of $Na^+$/$H^+$ antiporter confers salt tolerance on a fresh water cyanobacterium, making it capable of growth in sea water. Proc. Natl. Acad. Sci. USA 99, 4109-4114
  31. Waditee, R., Hibino, T., Tanaka, Y., Nakamura, T., Incharoensakdi, A. and Takabe, T. (2001) Halotolerant cyanobacterium Aphanothece halophytica contains an $Na^+$/$H^+$ antiporter, homologous to eukaryotic ones, with novel ion specificity affected by C-terminal tail. J. Biol. Chem. 276, 36931-36938 https://doi.org/10.1074/jbc.M103650200

피인용 문헌

  1. Reduced isotope fractionation by denitrification under conditions relevant to the ocean vol.92, 2012, https://doi.org/10.1016/j.gca.2012.05.020
  2. Development of Media for the Cultivation of Enterobacter amnigenus GG0461 and its Nitrate Uptake vol.54, pp.4, 2011, https://doi.org/10.3839/jabc.2011.041
  3. Na+-stimulated nitrate uptake with increased activity under osmotic upshift in Synechocystis sp. strain PCC 6803 vol.27, pp.10, 2011, https://doi.org/10.1007/s11274-011-0706-6