Anaerobic acclimation in Chlamydomonas reinhardtii: Anoxic gene expression, hydrogenase induction, and metabolic pathways

Journal of Biological Chemistry

Volumn 282, Issue 35, 2007, Pages 25475-25486

  Mus, Florence ^a   Dubini, Alexandra ^b,c   Seibert, Michael ^b   Posewitz, Matthew C ^b,c   Grossman, Arthur R ^a  

^a GEOPHYSICAL LABORATORY   (United States)

^b NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

^c Department of Geology and Geological Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROBIC DIGESTION; DNA; ENZYMES; GENE EXPRESSION; METABOLISM; PHOTOSYNTHETIC MEMBRANES;

ANAEROBIC ACCLIMATION; CELLULAR ENERGY; CHLAMYDOMONAS DNA MICROARRAYS;

MICROORGANISMS;

CATALASE; HYBRID PROTEIN; HYDROGEN; HYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEINASE;

ACCLIMATIZATION; ANOXIA; ARTICLE; CELL ENERGY; CELL HYPOXIA; CHLAMYDOMONAS REINHARDTII; CONTROLLED STUDY; DNA MICROARRAY; ENZYME INDUCTION; GENE EXPRESSION; METABOLISM; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

ACCLIMATIZATION; ALGAL PROTEINS; ANIMALS; CHLAMYDOMONAS REINHARDTII; CIRCADIAN RHYTHM; ENERGY METABOLISM; ETHANOL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME, PROTOZOAN; HYDROGEN; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXYGEN CONSUMPTION; PHOTOSYNTHESIS; POLYMERASE CHAIN REACTION; PROTOZOAN PROTEINS; TRANSCRIPTION, GENETIC;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; EUKARYOTA; PROKARYOTA;

EID: 34548489862     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M701415200     Document Type: Article

References (80)

1. Dent, R. M., Haglund, C. M., Chin, B. L., Kobayashi, M. C., and Niyogi, K. K. (2005) Plant Physiol. 137, 545-556
2. Ghirardi, M. L., King, P. W., Posewitz, M. C., Maness, P. C., Fedorov, A., Kim, K., Cohen, J., Schulten, K., and Seibert, M. (2005) Biochem. Soc. Trans. 33, 70-72
3. Ghirardi, M. L., Posewitz, M. C., Maness, P.-C., Dubini, A., Yu, J., and Seibert, M. (2007) Annu. Rev. Plant Biol. 58, 71-91
4. Happe, T., Hemschemeier, A., Winkler, M., and Kaminski, A. (2002) Trends Plant Sci. 7, 246-250
5. Harris, E. H. (1989) The Chlamydomonas Sourcebook. A Comprehensive Guide to Biology and Laboratory Use, Academic Press, San Diego
6. Harris, E. H. (2001) Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 363-406
7. Im, C. S., Zhang, Z., Shrager, J., Chang, C. W., and Grossman, A. R. (2003) Photosynth. Res. 75, 111-125
8. Kruse, O., Rupprecht, J., Bader, K. P., Thomas-Hall, S., Schenk, P. M., Finazzi, G., and Hankamer, B. (2005) J. Biol. Chem. 280, 34170-34177
9. Melis, A., Zhang, L., Forestier, M., Ghirardi, M. L., and Seibert, M. (2000) Plant Physiol. 122, 127-136
10. Moseley, J. L., Chang, C. W., and Grossman, A. R. (2006) Eukaryot. Cell 5, 26-44
11. Rochaix, J. D. (2002) FEBS Lett. 529, 34-38
12. Snell, W. J., Pan, J., and Wang, Q. (2004) Cell 117, 693-697
13. Moseley, J., Quinn, J., Eriksson, M., and Merchant, S. (2000) EMBO J. 19, 2139-2151
14. Quinn, J. M., Eriksson, M., Moseley, J. L., and Merchant, S. (2002) Plant Physiol. 128, 463-471
15. Steunou, A. S., Bhaya, D., Bateson, M. M., Melendrez, M. C., Ward, D. M., Brecht, E., Peters, J. W., Kuhl, M., and Grossman, A. R. (2006) Proc. Natl. Acad. Sci. U. S. A. 103, 2398-2403
16. Atteia, A., van Lis, R., Gelius-Dietrich, G., Adrait, A., Garin, J., Joyard, J., Rolland, N., and Martin, W. (2006) J. Biol. Chem. 281, 9909-9918
17. Hemschemeier, A., and Happe, T. (2005) Biochem. Soc. Trans 33, 39-41
18. Forestier, M., King, P., Zhang, L., Posewitz, M., Schwarzer, S., Happe, T., Ghirardi, M. L., and Seibert, M. (2003) Eur. J. Biochem. 270, 2750-2758
19. Happe, T., and Kaminski, A. (2002) Eur. J. Biochem. 269, 1022-1032
20. Posewitz, M. C., King, P. W., Smolinski, S. L., Smith, R. D., Ginley, A. R., Ghirardi, M. L., and Seibert, M. (2005) Biochem. Soc. Trans. 33, 102-104
21. Posewitz, M. C., King, P. W., Smolinski, S. L., Zhang, L., Seibert, M., and Ghirardi, M. L. (2004) J. Biol. Chem. 279, 25711-25720
22. Grossman, A. R., Croft, M., Gladyshev, V. N., Merchant, S. S., Posewitz, M. C., Prochnik, S., and Spalding, M. H. (2007) Curr. Opin. Plant Biol. 10, 190-198
23. Gfeller, R. P., and Gibbs, M. (1984) Plant Physiol. 75, 212-218
24. Ghirardi, M. L. (1997) Appl. Biochem. Biotechnol. 63, 141-151
25. Greenbaum, E. R., Guillard, R. L., and Sunda, W. G. (1983) Photochem. Photobiol. 37, 649-655
26. Posewitz, M. C., Smolinski, S. L., Kanakagiri, S., Melis, A., Seibert, M., and Ghirardi, M. L. (2004) Plant Cell 16, 2151-2163
27. Kosourov, S., Seibert, M., and Ghirardi, M. L. (2003) Plant Cell Physiol. 44, 146-155
28. Kosourov, S., Tsygankov, A., Seibert, M., and Ghirardi, M. L. (2002) Biotechnol. Bioeng. 78, 731-740
29. Zhang, L., Happe, T., and Melis, A. (2002) Planta 214, 552-561
30. Wykoff, D. D., Davies, J. P., Melis, A., and Grossman, A. R. (1998) Plant Physiol. 117, 129-139
31. Kreutzberg, K. (1984) Physiologia Plantarum 61, 87-94
32. Ohta, S., Miyamoto, K., and Miura, Y. (1987) Plant Physiol. 83, 1022-1026
33. Wagner, A. F., Frey, M., Neugebauer, F. A., Schäfer, W., and Knappe, J. (1992) Proc. Natl. Acad. Sci. U. S. A. 89, 996-1000
34. Kennedy, R. A., Rumpho, M. E., and Fox, T. C. (1992) Plant Physiol. 100, 1-6
35. Ben-Amotz, A., and Avron, M. (1972) Plant Physiol. 49, 240-243
36. Kessler, E. (1974) in Algal Physiology and Biochemistry: Botanical Monograph (Stewart, W. D. P., ed) Vol. 10, pp. 456-473, Blackwell Scientific, Oxford, UK
37. Klein, U., and Betz, A. (1978) Plant Physiol. 61, 953-956
38. Weaver, P. F., Lien, S., and Seibert, M. (1980) Solar Energy 24, 3-45
39. Happe, T., Mosler, B., and Naber, J. D. (1994) Eur. J. Biochem. 222, 769-774
40. Happe, T., and Naber, J. D. (1993) Eur. J. Biochem. 214, 475-481
41. Roessler, P. G., and Lien, S. (1984) Plant Physiol. 76, 1086-1089
42. Graves, D. A., Tevault, C. V., and Greenbaum, E. (1989) Photochem. Photobiol. 50, 571-576
43. Antal, T. K., Krendeleva, T. E., Laurinavichene, T. V., Makarova, V. V., Ghirardi, M. L., Rubin, A. B., Tsygankov, A. A., and Seibert, M. (2003) Biochim. Biophys. Acta 1607, 153-160
44. Kosourov, S., Makarova, V., Fedorov, A. S., Tsygankov, A., Seibert, M., and Ghirardi, M. L. (2005) Photosynth. Res. 85, 295-305
45. Fedorov, A., Kosourov, S., Ghirardi, M., and Seibert, M. (2005) Appl. Biochem. Biotechnol. 121, 403-412
46. Livak, K. J., and Schmittgen, T. D. (2001) Methods (Amsterdam) 25, 402-408
47. Eberhard, S., Jain, M., Im, C. S., Pollock, S., Shrager, J., Lin, Y., Peek, A. S., and Grossman, A. R. (2006) Curr. Genet 49, 106-124
48. Wanka, F., Joosten, H. F., and de Grip, W. J. (1970) Arch. Microbiol. 75, 25-36
49. Müller, M. (1993) J. Gen. Microbiol. 139, 2879-2889
50. Müller, M. (1998) in Evolutionary Relationships among Protozoa (Coombs, G. H., Vickerman, K., Sleigh, M. A., and Warren, A., eds) pp. 109-127, Kluwer Academic, Dordrecht, The Netherlands
51. Im, C. S., Eberhard, S., Huang, K., Beck, C. F., and Grossman, A. R. (2006) Plant J. 48, 1-16
52. Klok, E. J., Wilson, I. W., Wilson, D., Chapman, S. C., Ewing, R. M., Somerville, S. C., Peacock, W. J., Dolferus, R., and Dennis, E. S. (2002) Plant Cell 14, 2481-2494
53. Liu, F., Vantoai, T., Moy, L. P., Bock, G., Linford, L. D., and Quackenbush, J. (2005) Plant Physiol. 137, 1115-1129
54. Semenza, G. L. (1999) Cell 98, 281-284
55. Gfeller, R. P., and Gibbs, M. (1985) Plant Physiol. 77, 509-511
56. Buis, J. M., and Broderick, J. B. (2005) Arch. Biochem. Biophys. 433, 288-296
57. Wolfe, M. T., Heo, J., Garavelli, J. S., and Ludden, P. W. (2002) J. Bacteriol. 184, 5898-5902
58. Aragao, D., Macedo, S., Mitchell, E. P., Romao, C. V., Liu, M. Y., Frazao, C., Saraiva, L. M., Xavier, A. V., LeGall, J., van Dongen, W. M., Hagen, W. R., Teixeira, M., Carrondo, M. A., and Lindley, P. (2003) J. Biol. Inorg. Chem. 8, 540-548
59. Macedo, S., Mitchell, E. P., Romao, C. V., Cooper, S. J., Coelho, R., Liu, M. Y., Xavier, A. V., LeGall, J., Bailey, S., Garner, D. C., Hagen, W. R., Teixeira, M., Carrondo, M. A., and Lindley, P. (2002) J. Biol. Inorg. Chem. 7, 514-525
60. Ragsdale, S. W. (2004) Crit. Rev. Biochem. Mol. Biol. 39, 165-195
61. Almeida, C. C., Romao, C. V., Lindley, P. F., Teixeira, M., and Saraiva, L. M. (2006) J. Biol. Chem. 281, 32445-32450
62. Valentine, R. C., and Wolfe, R. S. (1963) J. Bacteriol. 85, 1114-1120
63. Douce, R., and Neuburger, M. (1999) Curr. Opin. Plant Biol. 2, 214-222
64. Reymond, P., Weber, H., Damond, M., and Farmer, E. E. (2000) Plant Cell 12, 707-720
65. Schenk, P. M., Kazan, K., Wilson, I., Anderson, J. P., Richmond, T., Somerville, S. C., and Manners, J. M. (2000) Proc. Natl. Acad. Sci. U. S. A. 97, 11655-11660
66. Seki, M., Narusaka, M., Abe, H., Kasuga, M., Yamaguchi-Shinozaki, K., Carninci, P., Hayashizaki, Y., and Shinozaki, K. (2001) Plant Cell 13, 61-72
67. Vignais, P. M., and Colbeau, A. (2004) Curr. Issues Mol. Biol. 6, 159-188
68. Rochaix, J. D., Perron, K., Dauvillée, D., Laroche, F., Takahashi, Y., and Goldschmidt-Clermont, M. (2004) Biochem. Soc. Trans. 32, 567-570
69. Rochaix, J. D. (2004) Plant Cell 16, 1650-1660
70. Dauvillée, D., Stampacchia, O., Girard-Bascou, J., and Rochaix, J. D. (2003) EMBO J. 22, 6378-6388
71. Tedin, K., and Norel, F. (2001) J. Bacteriol. 183, 6184-6196
72. Eichel, J., Chang, Y. Y., Riesenberg, D., and Cronan, J. E., Jr. (1999) J. Bacteriol. 181, 572-576
73. King, P. W., and Przybyla, A. E. (1999) J. Bacteriol. 181, 5250-5256
74. Bohne, A. V., Irihimovitch, V., Weihe, A., and Stern, D. B. (2006) Curr. Genet 49, 333-340
75. Kaska, D. D., Gunzler, V., Kivirikko, K. I., and Myllyla, R. (1987) Biochem. J. 241, 483-490
76. Hieta, R., and Myllyharju, J. (2002) J. Biol. Chem. 277, 23965-23971
77. Ivan, M., Kondo, K., Yang, H., Kim, W., Valiando, J., Ohh, M., Salic, A., Asara, J. M., Lane, W. S., and Kaelin, W. G., Jr. (2001) Science 292, 464-468
78. McDonough, M. A., Li, V., Flashman, E., Chowdhury, R., Mohr, C., Lienard, B. M., Zondlo, J., Oldham, N. J., Clifton, I. J., Lewis, J., McNeill, L. A., Kurzeja, R. J., Hewitson, K. S., Yang, E., Jordan, S., Syed, R. S., and Schofield, C. J. (2006) Proc. Natl. Acad. Sci. U. S. A. 103, 9814-9819
79. Gonzali, S., Loreti, E., Novi, G., Poggi, A., Alpi, A., and Perata, P. (2005) Ann. Bot. (Lond.) 96, 661-668
80. Sedbrook, J. C., Kronebusch, P. J., Borisy, G. G., Trewavas, A. J., and Masson, P. H. (1996) Plant Physiol. 111, 243-257