Physiological role and regulation of glutamate dehydrogenase in Prochlorococcus sp. strain MIT9313

Environmental Microbiology Reports

Volumn 1, Issue 1, 2009, Pages 56-64

  Rangel, Oriol Alberto ^a   Gómez Baena, Guadalupe ^a   López Lozano, Antonio ^a   Diez, Jesús ^a   García Fernández, Jose Manuel ^a  

^a UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROCHLOROCOCCUS; PROCHLOROCOCCUS SP.;

EID: 66749127417     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/j.1758-2229.2008.00005.x     Document Type: Article

References (67)

1. Boussiba, S., Resch, C.M., and Gibson, J. (1984) Ammonia uptake and retention in some cyanobacteria. Arch Microbiol 138: 287-292.
2. Carrigan, J.B., Coughlan, S., and Engel, P.C. (2005) Properties of the thermostable glutamate dehydrogenase of the mesophilic anaerobe Peptostreptoccus asaccharolyticus purified by a novel method after over-expression in an Escherichia coli host. FEMS Microbiol Let 244: 53-59.
3. Chisholm, S.W., Olson, R.J., Zettler, E.R., Goericke, R., Waterbury, J.B., and Welschmeyer, N.A. (1988) A novel free living prochlorophyte abundant in the oceanic euphotic zone. Nature 334: 340-343.
4. Chisholm, S.W., Frankel, S.L., Goericke, R., Olson, R.J., Palenik, B., Waterbury, J.B., et al. (1992) Prochlorococcus marinus nov. gen. nov. sp.: an oxyphototrophic marine prokaryote containing divinyl chlorophyll a and chlorophyll b. Arch Microbiol 157: 297-300.
5. Chávez, S., and Candau, P. (1991) An NAD-specific glutamate dehydrogenase from cyanobacteria. Identification and properties. FEBS Let 285: 35-38.
6. Chávez, S., Reyes, J.C., Chauvat, F., Florencio, F.J., and Candau, P. (1995) The NADP-glutamate dehydrogenase of the cyanobacterium Synechocystis 6803 cloning, transcriptional analysis and disruption of the gdhA gene. Plant Mol Biol 28: 173-188.
7. Chávez, S., Lucena, J.M., Reyes, J.C., Florencio, F.J., and Candau, P. (1999) The presence of glutamate dehydrogenase is a selective advantage for the cyanobacterium Synechocystis sp. strain PCC-6803 under nonexponential growth conditions. J Bacteriol 181: 808-813.
8. Choudhury, R., and Punekar, N.S. (2007) Competitive inhibition of glutamate dehydrogenase reaction. FEBS Let 581: 2733-2736.
9. Coleman, M.L., and Chisholm, S.W. (2007) Code and context: prochlorococcus as a model for cross-scale biology. Trends Microbiol 15: 398-407.
10. Coleman, M.L., Sullivan, M.B., Martiny, A.C., Steglich, C., Barry, K., Delong, E.F., and Chisholm, S.W. (2006) Genomic islands and the ecology and evolution of Prochlorococcus. Science 311: 1768-1770.
11. Coulton, J.W., and Kapoor, M. (1973) Studies on the kinetics and regulation of glutamate dehydrogenase of Salmonella typhimurium. Can J Microbiol 19: 439-450.
12. Cullimore, J.V., and Sims, A.P. (1981) Pathway of ammonia assimilation in illuminated and darkened Chlamydomonas reinhardii. Phytochemistry 20: 933-940.
13. DeLuna, A., Avendaño, A., Riego, L., and González, A. (2001) NADP-glutamate dehydrogenase isoenzymes of Saccharomyces cerevisiae. Purification, kinetic properties, and physiological roles. J Biol Chem 276: 43775-43783.
14. Diaz, S., Perez-Pomares, F., Pire, C., Ferrer, J., and Bonete, M.J. (2006) Gene cloning, heterologous overexpression and optimized refolding of the NAD-glutamate dehydrogenase from Haloferax mediterranei. Extremophiles 10: 105-115.
15. Diez, J., and López-Ruiz, A. (1989) Immunological approach to the regulation of nitrate reductase in Monoraphidium braunii. Arch Biochem Biophys 268: 707-715.
16. Dufresne, A., Salanoubat, M., Partensky, F., Artiguenave, F., Axmann, I.M., Barbe, V., et al. (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 100: 10020-10025.
17. El Alaoui, S., Diez, J., Humanes, L., Toribio, F., Partensky, F., and García-Fernández, J.M. (2001) In vivo regulation of glutamine synthetase activity in the marine chlorophyll b-containing cyanobacterium Prochlorococcus sp. strain PCC 9511 (Oxyphotobacteria). Appl Environ Microbiol 67: 2202-2207.
18. El Alaoui, S., Diez, J., Toribio, F., Gómez-Baena, G., Dufresne, A., and García-Fernández, J.M. (2003) Glutamine synthetase from the marine cyanobacteria Prochlorococcus spp.: characterization, phylogeny and response to nutrient limitation. Environ Microbiol 5: 412-423.
19. Florencio, F.J., Marques, S., and Candau, P. (1987) Identification and characterization of a glutamate dehydrogenase in the unicellular cyanobacterium Synechocystis PCC 6803. FEBS Let 223: 37-41.
20. Follows, M.J., Dutkiewicz, S., Grant, S., and Chisholm, S.W. (2007) Emergent biogeography of microbial communities in a model ocean. Science 315: 1843-1846.
21. García-Fernández, J.M., Tandeau de Marsac, N., and Diez, J. (2004) Streamlined regulation and gene loss as adaptive mechanisms in Prochlorococcus for optimized nitrogen utilization in oligotrophic environments. Microbiol Mol Biol Rev 68: 630-638.
22. Goericke, R., and Welschmeyer, N.A. (1993) The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep Sea Res I 40: 2283-2294.
23. Goericke, R., Olson, R.J., and Shalapyonok, A. (2000) A novel niche for Prochlorococcus sp. in low-light suboxic environments in the Arabian Sea and the Eastern Tropical North Pacific. Deep Sea Res I 47: 1183-1205.
24. Gómez-Baena, G., García-Fernández, J.M., Lopez-Lozano, A., Toribio, F., and Diez, J. (2006) Glutamine synthetase degradation is controlled by oxidative proteolysis in the marine cyanobacterium Prochlorococcus marinus strain PCC 9511. Biochim Biophys Acta 1760: 930-940.
25. Gómez-Baena, G., López-Lozano, A., Gil-Martínez, J., Lucena, J.M., Diez, J., Candau, P., and García-Fernández, J.M. (2008) Glucose uptake and its effect on gene expression in Prochlorococcus. PLoS ONE 3: e3416.
26. Hayden, B.M., Bonete, M.J., Brown, P.E., Moir, A.J., and Engel, P.C. (2002) Glutamate dehydrogenase of Halobacterium salinarum: evidence that the gene sequence currently assigned to the NADP+-dependent enzyme is in fact that of the NAD+-dependent glutamate dehydrogenase. FEMS Microbiol Let 211: 37-41.
27. Helling, R.B. (1994) Why does Escherichia coli have two primary pathways for synthesis of glutamate? J Bacteriol 176: 4664-4668.
28. Helling, R.B. (1998) Pathway choice in glutamate synthesis in Escherichia coli. J Bacteriol 180: 4571-4575.
29. Hoare, D.S., Hoare, S.L., and Moore, R.B. (1967) The photoassimilation of organic compounds by autotrophic blue-green algae. J Gen Microbiol 49: 351-370.
30. Hudson, R.C., Ruttersmith, L.D., and Daniel, R.M. (1993) Glutamate-dehydrogenase from the extremely thermophilic archaebacterial isolate An1. Biochim Biophys Acta 1202: 244-250.
31. Inokuchi, R., Itagaki, T., Wiskich, J.T., Nakayama, K., and Okada, M. (1997) An NADP-glutamate dehydrogenase from the green alga Bryopsis maxima. Purification and properties. Plant Cell Physiol 38: 327-335.
32. Johnson, Z., Landry, M.L., Bidigare, R.R., Brown, S.L., Campbell, L., Gunderson, J., et al. (1999) Energetics and growth-kinetics of a deep Prochlorococcus spp. population in the Arabian-Sea. Deep Sea Res II 46: 1719-1743.
33. Kettler, G.C., Martiny, A.C., Huang, K., Zucker, J., Coleman, M.L., Rodrigue, S., et al. (2007) Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genetics 3: 2515-2528.
34. Kim, Y.-J., Yoshizawa, M., Takenaka, S., Murakami, S., and Aoki, K. (2002) Ammonia assimilation in Klebsiella pneumoniae F-5-2 that can utilize ammonium and nitrate ions simultaneously: purification and characterization of glutamate dehydrogenase and glutamine synthetase. J Biosci Bioeng 93: 584-588.
35. Lea, P.J., and Miflin, B.J. (1974) Alternative route for nitrogen assimilation in higher-plants. Nature 251: 614-616.
36. Liu, H.B., Nolla, H.A., and Campbell, L. (1997) Prochlorococcus growth rate and contribution to primary production in the Equatorial and Subtropical North Pacific ocean. Aquat Microb Ecol 12: 39-47.
37. López-Lozano, A., Diez, J., El Alaoui, S., Moreno-Vivián, C., and García-Fernández, J.M. (2002) Nitrate is reduced by heterotrophic bacteria but not transferred to Prochlorococcus in non axenic cultures. FEMS Microbiol Ecol 41: 151-160.
38. Martínez-Bilbao, M., Martínez, A., Urkijo, I., Llama, M.J., and Serra, J.L. (1988) Induction, isolation, and some properties of the NADPH-dependent glutamate dehydrogenase from the nonheterocystous cyanobacterium Phormidium laminosum. J Bacteriol 170: 4897-4902.
39. Mary, I., Tarran, G.A., Warwick, P.E., Terry, M.J., Scanlan, D.J., Burkill, P.H., and Zubkov, M.V. (2008a) Light enhanced amino acid uptake by dominant bacterioplankton groups in surface waters of the Atlantic Ocean. FEMS Microbiol Ecol 63: 36-45.
40. Mary, I., Garczarek, L., Tarran, G.A., Kolowrat, C., Terry, M.J., Scanlan, D.J., et al. (2008b) Diel rhythmicity in amino acid uptake by Prochlorococcus. Environ Microbiol 10: 2124-2131.
41. Meeks, J.C. (1981) Radiotracer studies of nitrogen metabolism in cyanobacteria. In Short-lived Radionuclides in Chemistry and Biology. Root, J.W., and Krohn, K.A. (eds). Washington, DC, USA: American Chemical Society, pp. 269-293.
42. Michelou, V.K., Cottrell, M.T., and Kirchman, D.L. (2007) Lightstimulated bacterial production and amino acid assimilation by cyanobacteria and other microbes in the North Atlantic Ocean. Appl Environ Microbiol 73: 5539-5546.
43. Moyano, E., Cárdenas, J., and Muñoz-Blanco, J. (1992) Purification and properties of three NAD(P)+ isozymes of L-glutamate dehydrogenase of Chlamydomonas reinhardtii. Biochim Biophys Acta 1119: 63-68.
44. Mérida, A., Candau, P., and Florencio, F.J. (1991) Regulation of glutamine synthetase activity in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803 by the nitrogen source: effect of ammonium. J Bacteriol 173: 4095-4100.
45. Pace, J., and McDermott, E.E. (1952) Methionine sulphoximine and some enzyme systems involving glutamine. Nature 169: 415-416.
46. Palenik, B., Brahamsha, B., Larimer, F., Land, M., Hauser, L., Chain, P., et al. (2003) The genome of a motile marine Synechococcus. Nature 424: 1037-1042.
47. Partensky, F., Hess, W.R., and Vaulot, D. (1999a) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106-127.
48. Partensky, F., Blanchot, J., and Vaulot, D. (1999b) Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. In Marine Cyanobacteria. Charpy, L., and Larkum, A.W.D. (eds). Monaco, Monaco: Bulletin de l'Institut Océanographique, Numéro spécial, pp. 457-476.
49. Pinkus, L.M. (1977) Glutamine binding sites. Methods Enzymol 46: 414-427.
50. Post, A.F. (2005) Nutrient limitation of marine cyanobacteria. In Harmful Cyanobacteria. Huisman, J., Matthijs, H., and Visser, P.M. (eds). Dordrecht, the Netherlands: Kluwer Academic Publisher.
51. Rhodes, D., Rich, P.J., and Brunk, D.G. (1989) Amino acid metabolism of Lemna minor L.: IV. N-labeling kinetics of the amide and amino groups of glutamine and asparagine. Plant Physiol 89: 1161-1171.
52. Rocap, G., Larimer, F.W., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N.A., et al. (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042-1047.
53. Ruiz, J.L., Ferrer, J., Pire, C., Llorca, F.I., and Bonete, M.J. (2003) Denaturation studies by fluorescence and quenching of thermophilic protein NAD+-glutamate dehydrogenase from Thermus thermophilus HB8. J Prot Chem 22: 295-301.
54. Sallala, A.-K.J., and Nimera, N.A. (1990) The presence of glutamate dehydrogenase in Chlorogloeopsis fritschii. FEMS Microbiol Lett 67: 215-220.
55. Scheid, H.W., Ehmke, A., and Hartman, T. (1980) Plant NAD-dependent glutamate dehydrogenase. Purification, molecular properties and metal ion activation of the enzymes from Lemna minor and Pisum sativum. Z Naturforsch [C] 35: 213-221.
56. Skoku, T.A., Wolk, C.P., Meeks, J.C., and Schaffer, P.W. (1978) Initial organic products of assimilation of [13N]-ammonium and [13N]-nitrate by tobacco cells cultured on different sources of nitrogen. Plant Physiol 62: 299-304.
57. Smith, E.L., Austen, B.M., Blumenthal, K.M., and Nyc, J.F. (1975) Glutamate Dehydrogenase. New York, NY, USA: Academic Press.
58. Stewart, G.R., Mann, A.F., and Fentem, P.A. (1980) Enzymes of Glutamate Formation: Glutamate Dehydrogenase, Glutamine Synthetase, and Glutamate Synthase. New York, NY, USA: Academic Press.
59. Tolonen, A.C., Aach, J., Lindell, D., Johnson, Z.I., Rector, T., Steen, R., et al. (2006) Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability. Mol Sys Biol 2: 53.
60. Turpin, D.H., Elrifi, I.R., Birch, D.G., Weger, H.G., and Holmes, J.J. (1988) Interactions between photosynthesis, respiration, and nitrogen assimilation in microalgae. Can J Bot 66: 2083-2097.
61. Yoneyama, T., and Kumazawa, K. (1974) Kinetic study of assimilation of N-15-labelled ammonium in rice seedling roots. Plant Cell Physiol 15: 655-661.
62. Zahradnícková, H., Husek, P., Simek, P., Hartvich, P., Marsálek, B., and Holoubeck, I. (2007) Determination of D-and L-amino acids produced by cyanobacteria using gas chromatography on Chirasil-Val after derivatization with pentafluoropropyl chloroformate. Anal Bioanal Chem 388: 1815-1822.
63. Zinser, E.R., Coe, A., Johnson, Z.I., Martiny, A.C., Fuller, N.J., Scanlan, D.J., and Chisholm, S.W. (2006) Prochlorococcus ecotype abundances in the north atlantic ocean as revealed by an improved quantitative PCR method. Appl Environ Microbiol 72: 723-732.
64. Zubkov, M.V., and Tarran, G.A. (2005) Amino acid uptake of Prochlorococcus spp. in surface waters across the South Atlantic Subtropical Front. Aquat Microb Ecol 40: 241-249.
65. Zubkov, M.V., Fuchs, B.M., Tarran, G.A., Burkill, P.H., and Amann, R. (2003) High rate of uptake of organic nitrogen compounds by Prochlorococcus cyanobacteria as a key to their dominance in oligotrophic oceanic waters. Appl Environ Microbiol 69: 1299-1304.
66. Zubkov, M.V., Tarran, G.A., and Fuchs, B.M. (2004) Depth related amino acid uptake by Prochlorococcus cyanobacteria in the Southern Atlantic tropica gyre. FEMS Microbiol Ecol 50: 153-161.
67. Zwirglmaier, K., Jardillier, L., Ostrowski, M., Mazard, S., Garczarek, L., Vaulot, D., et al. (2007) Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 10: 147-161.