New insights into Chlamydomonas reinhardtii hydrogen production processes by combined microarray/RNA-seq transcriptomics

Plant Biotechnology Journal

Volumn 11, Issue 6, 2013, Pages 717-733

  Toepel, Jörg ^a   Illmer Kephalides, Maike ^a   Jaenicke, Sebastian ^a   Straube, Jasmin ^a   May, Patrick ^b   Goesmann, Alexander ^a   Kruse, Olaf ^a  

^a BIELEFELD UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

Chlamydomonas reinhardtii; Hydrogen production; Transcriptomics

Indexed keywords

CHLAMYDOMONAS REINHARDTII;

EID: 84881029054     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12062     Document Type: Article

References (79)

1. Baurain, D., Dinant, M., Coosemans, N. and Matagne, R.F. (2003) Regulation of the alternative oxidase Aox1 gene in Chlamydomonas reinhardtii. Role of the nitrogen source on the expression of a reporter gene under the control of the Aox1 promoter. Plant Physiol. 131, 1418-1430.
2. Blom, J., Jakobi, T., Doppmeier, D., Jaenicke, S., Kalinowski, J., Stoye, J. and Goesmann, A. (2011) Exact and complete short-read alignment to microbial genomes using Graphics Processing Unit programming. Bioinformatics, 27, 1351-1358.
3. Bonente, G., Ballottari, M., Truong, T.B., Morosinotto, T., Ahn, T.K., Fleming, G.R., Niyogi, K.K. and Bassi, R. (2011) Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLoS Biol. 9, 107-110.
4. Boyle, N.R., Page, M.D., Liu, B., Blaby, I.K., Casero, D., Kropat, J., Cokus, S.J., Hong-Hermesdorf, A., Shaw, J., Karpowicz, S.J., Gallaher, S.D., Johnson, S., Benning, C., Pellegrini, M., Grossman, A. and Merchant, S.S. (2012) Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas. J. Biol. Chem. 287, 15811-15825.
5. Carol, P. and Kuntz, M. (2001) A plastid terminal oxidase comes to light: implications for carotenoid biosynthesis and chlororespiration. Trends Plant Sci. 6, 31-36.
6. Catalanotti, C., Dubini, A., Subramanian, V., Yang, W.Q., Magneschi, L., Mus, F., Seibert, M., Posewitz, M.C. and Grossman, A.R. (2012) Altered fermentative metabolism in Chlamydomonas reinhardtii mutants lacking pyruvate formate lyase and both pyruvate formate lyase and alcohol dehydrogenase. Plant Cell, 24, 692-707.
7. Chen, M., Zhao, L., Sun, Y.L., Cui, S.X., Zhang, L.F., Yang, B., Wang, J., Kuang, T.Y. and Huang, F. (2010) Proteomic analysis of hydrogen photoproduction in sulfur-deprived Chlamydomonas cells. J. Proteome Res. 9, 3854-3866.
8. Chochois, V., Dauvillee, D., Beyly, A., Tolleter, D., Cuine, S., Timpano, H., Ball, S., Cournac, L. and Peltier, G. (2009) Hydrogen production in Chlamydomonas: photosystem II-dependent and -independent pathways differ in their requirement for starch metabolism. Plant Physiol. 151, 631-640.
9. Chochois, V., Constans, L., Dauvillee, D., Beyly, A., Soliveres, M., Ball, S., Peltier, G. and Cournac, L. (2010) Relationships between PSII-independent hydrogen bioproduction and starch metabolism as evidenced from isolation of starch catabolism mutants in the green alga Chlamydomonas reinhardtii. Int. J. Hydrogen Energy, 35, 10731-10740.
10. Desplats, C., Mus, F., Cuine, S., Billon, E., Cournac, L. and Peltier, G. (2009) Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts. J. Biol. Chem. 284, 4148-4157.
11. Dietz, K.J. (2003) Redox control, redox signaling, and redox homeostasis in plant cells. Int. Rev. Cytol. 228, 141-193.
12. Dietz, K.J. (2010) Redox-dependent regulation, redox control and oxidative damage in plant cells subjected to abiotic stress. Methods Mol. Biol. 639, 57-70.
13. 2 production in Chlamydomonas reinhardtii. J. Biol. Chem. 285, 30247-30260.
14. Eberhard, S., Jain, M., Im, C.S., Pollock, S., Shrager, J., Lin, Y., Peek, A.S. and Grossman, A.R. (2006) Generation of an oligonucleotide array for analysis of gene expression in Chlamydomonas reinhardtii. Curr. Genet. 49, 106-124.
15. Eberhard, S., Loiselay, C., Drapier, D., Bujaldon, S., Girard-Bascou, J., Kuras, R., Choquet, Y. and Wollman, F.A. (2011) Dual functions of the nucleus-encoded factor TDA1 in trapping and translation activation of atpA transcripts in Chlamydomonas reinhardtii chloroplasts. Plant J. 67, 1055-1066.
16. Eroglu, E. and Melis, A. (2011) Photobiological hydrogen production: recent advances and state of the art. Bioresour. Technol. 102, 8403-8413.
17. Esper, B., Badura, A. and Rogner, M. (2006) Photosynthesis as a power supply for (bio-)hydrogen production. Trends Plant Sci. 11, 543-549.
18. 2-concentrating mechanism regulator CIA5/CCM1. Plant Cell, 24, 1876-1893.
19. Fischer, B.B., Ledford, H.K., Wakao, S., Huang, S.G., Casero, D., Pellegrini, M., Merchant, S.S., Koller, A., Eggen, R.I.L. and Niyogi, K.K. (2012) SINGLET OXYGEN RESISTANT 1 links reactive electrophile signaling to singlet oxygen acclimation in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 109, E1302-E1311.
20. Gonzalez-Ballester, D., Casero, D., Cokus, S., Pellegrini, M., Merchant, S.S. and Grossman, A.R. (2010) RNA-seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell, 22, 2058-2084.
21. Gonzalez-Ballester, D., Pootakham, W., Mus, F., Yang, W., Catalanotti, C., Magneschi, L., de Montaigu, A., Higuera, J.J., Prior, M., Galvan, A., Fernandez, E. and Grossman, A.R. (2011) Reverse genetics in Chlamydomonas: a platform for isolating insertional mutants. Plant Methods, 7, 24.
22. Grossman, A.R., Catalanotti, C., Yang, W.Q., Dubini, A., Magneschi, L., Subramanian, V., Posewitz, M.C. and Seibert, M. (2011) Multiple facets of anoxic metabolism and hydrogen production in the unicellular green alga Chlamydomonas reinhardtii. New Phytol. 190, 279-288.
23. Happe, T. and Kaminski, A. (2002) Differential regulation of the Fe-hydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii. Eur. J. Biochem. 269, 1022-1032.
24. Happe, T., Hemschemeier, A., Winkler, M. and Kaminski, A. (2002) Hydrogenases in green algae: do they save the algae's life and solve our energy problems? Trends Plant Sci. 7, 246-250.
25. Harris, E.H. (1989) The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use. Oxford, UK: Academic Press.
26. Hemschemeier, A. and Happe, T. (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim. Biophys. Acta, 1807, 919-926.
27. Hemschemeier, A., Fouchard, S., Cournac, L., Peltier, G. and Happe, T. (2008a) Hydrogen production by Chlamydomonas reinhardtii: an elaborate interplay of electron sources and sinks. Planta, 227, 397-407.
28. Hemschemeier, A., Jacobs, J. and Happe, T. (2008b) Biochemical and physiological characterization of the pyruvate formate-lyase Pfl1 of Chlamydomonas reinhardtii, a typically bacterial enzyme in a eukaryotic alga. Eukaryot. Cell, 7, 518-526.
29. Kalamaki, M.S., Alexandrou, D., Lazari, D., Merkouropoulos, G., Fotopoulos, V., Pateraki, I., Aggelis, A., Carrillo-Lopez, A., Rubio-Cabetas, M.J. and Kanellis, A.K. (2009) Over-expression of a tomato N-acetyl-L-glutamate synthase gene (SlNAGS1) in Arabidopsis thaliana results in high ornithine levels and increased tolerance in salt and drought stresses. J. Exp. Bot. 60, 1859-1871.
30. 2 production in engineered green algal cells. J. Biol. Chem. 280, 34170-34177.
31. La Russa, M., Bogen, C., Uhmeyer, A., Doebbe, A., Filippone, E., Kruse, O. and Mussgnug, J.H. (2012) Functional analysis of three type-2 DGAT homologue genes for triacylglycerol production in the green microalga Chlamydomonas reinhardtii. J. Biotechnol. 162, 13-20.
32. Lecler, R., Godaux, D., Vigeolas, H., Hiligsmann, S., Thonart, P., Franck, F., Cardol, P. and Remacle, C. (2011) Functional analysis of hydrogen photoproduction in respiratory-deficient mutants of Chlamydomonas reinhardtii. Int. J. Hydrogen Energy, 36, 9562-9570.
33. Lehr, F., Morweiser, M., Sastre, R.R., Kruse, O. and Posten, C. (2012) Process development for hydrogen production with Chlamydomonas reinhardtii based on growth and product formation kinetics. J. Biotechnol. 162, 89-96.
34. Li, Z., Gao, J., Benning, C. and Sharkey, T.D. (2012) Characterization of photosynthesis in Arabidopsis ER-to-plastid lipid trafficking mutants. Photosynth. Res. 112, 49-61.
35. Liu, S., Lin, L., Jiang, P., Wang, D. and Xing, Y. (2011) A comparison of RNA-Seq and high-density exon array for detecting differential gene expression between closely related species. Nucleic Acids Res. 39, 578-588.
36. Lu, B., Xu, C., Awai, K., Jones, A.D. and Benning, C. (2007) A small ATPase protein of Arabidopsis, TGD3, involved in chloroplast lipid import. J. Biol. Chem. 282, 35945-35953.
37. Magneschi, L., Catalanotti, C., Subramanian, V., Dubini, A., Yang, W.Q., Mus, F., Posewitz, M.C., Seibert, M., Perata, P. and Grossman, A.R. (2012) A mutant in the ADH1 gene of Chlamydomonas reinhardtii elicits metabolic restructuring during anaerobiosis. Plant Physiol. 158, 1293-1305.
38. Malone, J.H. and Oliver, B. (2011) Microarrays, deep sequencing and the true measure of the transcriptome. BMC Biol. 9, 34.
39. Maruta, T., Tanouchi, A., Tamoi, M., Yabuta, Y., Yoshimura, K., Ishikawa, T. and Shigeoka, S. (2010) Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol. 51, 190-200.
40. 2 production by sulfur depletion. J. Biol. Chem. 284, 23415-23425.
41. Melis, A. and Happe, T. (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol. 127, 740-748.
42. Miller, R., Wu, G., Deshpande, R.R., Vieler, A., Gartner, K., Li, X., Moellering, E.R., Zauner, S., Cornish, A.J., Liu, B., Bullard, B., Sears, B.B., Kuo, M.H., Hegg, E.L., Shachar-Hill, Y., Shiu, S.H. and Benning, C. (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol. 154, 1737-1752.
43. Moharikar, S., D'Souza, J.S. and Rao, B.J. (2007) A homologue of the defender against the apoptotic death gene (dad1)in UV-exposed Chlamydomonas cells is downregulated with the onset of programmed cell death. J. Biosci. 32, 261-270.
44. Moroney, J.V., Ma, Y., Frey, W.D., Fusilier, K.A., Pham, T.T., Simms, T.A., DiMario, R.J., Yang, J. and Mukherjee, B. (2011) The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth. Res. 109, 133-149.
45. Msanne, J., Xu, D., Konda, A.R., Casas-Mollano, J.A., Awada, T., Cahoon, E.B. and Cerutti, H. (2012) Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochemistry, 75, 50-59.
46. Mus, F., Dubini, A., Seibert, M., Posewitz, M.C. and Grossman, A.R. (2007) Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathways. J. Biol. Chem. 282, 25475-25486.
47. Mussgnug, J.H., Klassen, V., Schluter, A. and Kruse, O. (2010) Microalgae as substrates for fermentative biogas production in a combined biorefinery concept. J. Biotechnol. 150, 51-56.
48. Nagy, V., Tengolics, R., Schansker, G., Rakhely, G., Kovacs, K.L., Garab, G. and Toth, S.Z. (2012) Stimulatory effect of ascorbate, the alternative electron donor of photosystem II, on the hydrogen production of sulphur-deprived Chlamydomonas reinhardtii. Int. J. Hydrogen Energy, 37, 8864-8871.
49. Nguyen, A.V., Thomas-Hall, S.R., Malnoe, A., Timmins, M., Mussgnug, J.H., Rupprecht, J., Kruse, O., Hankamer, B. and Schenk, P.M. (2008) Transcriptome for photobiological hydrogen production induced by sulfur deprivation in the green alga Chlamydomonas reinhardtii. Eukaryot. Cell, 7, 1965-1979.
50. 2 production. PLoS ONE, 6, e29364.
51. Niyogi, K.K., Bjorkman, O. and Grossman, A.R. (1997) Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell, 9, 1369-1380.
52. Oshlack, A., Robinson, M.D. and Young, M.D. (2010) From RNA-seq reads to differential expression results. Genome Biol. 11, 220.
53. Ossenbuhl, F. and Nickelsen, J. (2000) cis- and trans-Acting determinants for translation of psbD mRNA in Chlamydomonas reinhardtii. Mol. Cell. Biol. 20, 8134-8142.
54. Peers, G., Truong, T.B., Ostendorf, E., Busch, A., Elrad, D., Grossman, A.R., Hippler, M. and Niyogi, K.K. (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature, 462, 518-521.
55. Perez-Perez, M.E., Florencio, F.J. and Crespo, J.L. (2010) Inhibition of target of rapamycin signaling and stress activate autophagy in Chlamydomonas reinhardtii. Plant Physiol. 152, 1874-1888.
56. Philipps, G., Krawietz, D., Hemschemeier, A. and Happe, T. (2011) A pyruvate formate lyase-deficient Chlamydomonas reinhardtii strain provides evidence for a link between fermentation and hydrogen production in green algae. Plant J. 66, 330-340.
57. Philipps, G., Happe, T. and Hemschemeier, A. (2012) Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii. Planta, 235, 729-745.
58. Piao, L., Li, Y., Kim, S.J., Byun, H.S., Huang, S.M., Hwang, S.K., Yang, K.J., Park, K.A., Won, M., Hong, J., Hur, G.M., Seok, J.H., Shong, M., Cho, M.H., Brazil, D.P., Hemmings, B.A. and Park, J. (2009) Association of LETM1 and MRPL36 contributes to the regulation of mitochondrial ATP production and necrotic cell death. Cancer Res. 69, 3397-3404.
59. Prestele, M., Vogel, F., Reichert, A.S., Herrmann, J.M. and Ott, M. (2009) Mrpl36 is important for generation of assembly competent proteins during mitochondrial translation. Mol. Biol. Cell, 20, 2615-2625.
60. Ramskold, D., Kavak, E. and Sandberg, R. (2012) How to analyze gene expression using RNA-sequencing data. Methods Mol. Biol. 802, 259-274.
61. Roston, R.L., Gao, J., Murcha, M.W., Whelan, J. and Benning, C. (2012) TGD1, -2, and -3 proteins involved in lipid trafficking form ATP-binding cassette (ABC) transporter with multiple substrate-binding proteins. J. Biol. Chem. 287, 21406-21415.
62. Sano, S., Ueda, M., Kitajima, S., Takeda, T., Shigeoka, S., Kurano, N., Miyachi, S., Miyake, C. and Yokota, A. (2001) Characterization of ascorbate peroxidases from unicellular red alga Galdieria partita. Plant Cell Physiol. 42, 433-440.
63. 2 production in a Chlamydomonas reinhardtii D1 protein mutant. J. Biotechnol. 157, 613-619.
64. Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y. and Yoshimura, K. (2002) Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 53, 1305-1319.
65. Smith, D.R., Quinlan, A.R., Peckham, H.E., Makowsky, K., Tao, W., Woolf, B., Shen, L., Donahue, W.F., Tusneem, N., Stromberg, M.P., Stewart, D.A., Zhang, L., Ranade, S.S., Warner, J.B., Lee, C.C., Coleman, B.E., Zhang, Z., McLaughlin, S.F., Malek, J.A., Sorenson, J.M., Blanchard, A.P., Chapman, J., Hillman, D., Chen, F., Rokhsar, D.S., McKernan, K.J., Jeffries, T.W., Marth, G.T. and Richardson, P.M. (2008) Rapid whole-genome mutational profiling using next-generation sequencing technologies. Genome Res. 18, 1638-1642.
66. Steenvoorden, D.P. and van Henegouwen, G.M. (1997) The use of endogenous antioxidants to improve photoprotection. J. Photochem. Photobiol. B Biol. 41, 1-10.
67. Sturn, A., Quackenbush, J. and Trajanoski, Z. (2002) Genesis: cluster analysis of microarray data. Bioinformatics, 18, 207-208.
68. Takahara, K., Kasajima, I., Takahashi, H., Hashida, S.N., Itami, T., Onodera, H., Toki, S., Yanagisawa, S., Kawai-Yamada, M. and Uchimiya, H. (2010) Metabolome and photochemical analysis of rice plants overexpressing Arabidopsis NAD kinase gene. Plant Physiol. 152, 1863-1873.
69. Takeda, T., Ishikawa, T. and Shigeoka, S. (1997) Metabolism of hydrogen peroxide by the scavenging system in Chlamydomonas reinhardtii. Physiol. Plant. 99, 49-55.
70. Takeda, T., Yoshimura, K., Yoshii, M., Kanahoshi, H., Miyasaka, H. and Shigeoka, S. (2000) Molecular characterization and physiological role of ascorbate peroxidase from halotolerant Chlamydomonas sp W80 strain. Arch. Biochem. Biophys. 376, 82-90.
71. Toepel, J., Albaum, S.P., Arvidsson, S., Goesmann, A., la Russa, M., Rogge, K. and Kruse, O. (2011) Construction and evaluation of a whole genome microarray of Chlamydomonas reinhardtii. BMC Genomics, 12, 579.
72. Tolleter, D., Ghysels, B., Alric, J., Petroutsos, D., Tolstygina, I., Krawietz, D., Happe, T., Auroy, P., Adriano, J.M., Beyly, A., Cuine, S., Plet, J., Reiter, I.M., Genty, B., Cournac, L., Hippler, M. and Peltier, G. (2011) Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell, 23, 2619-2630.
73. Torzillo, G., Scoma, A., Faraloni, C., Ena, A. and Johanningmeier, U. (2009) Increased hydrogen photoproduction by means of a sulfur-deprived Chlamydomonas reinhardtii D1 protein mutant. Int. J. Hydrogen Energy, 34, 4529-4536.
74. Urzica, E.I., Adler, L.N., Page, M.D., Linster, C.L., Arbing, M.A., Casero, D., Pellegrini, M., Merchant, S.S. and Clarke, S.G. (2012) Impact of oxidative stress on ascorbate biosynthesis in Chlamydomonas via regulation of the VTC2 gene encoding a GDP-L-galactose phosphorylase. J. Biol. Chem. 287, 14234-14245.
75. Wang, Y., Ghaffari, N., Johnson, C.D., Braga-Neto, U.M., Wang, H., Chen, R. and Zhou, H. (2011) Evaluation of the coverage and depth of transcriptome by RNA-Seq in chickens. BMC Bioinformatics, 12(Suppl 10), S5.
76. Wang, Z., Xu, C. and Benning, C. (2012) TGD4 involved in endoplasmic reticulum-to-chloroplast lipid trafficking is a phosphatidic acid binding protein. Plant J. 70, 614-623.
77. Winkler, M., Hemschemeier, A., Jacobs, J., Stripp, S. and Happe, T. (2010) Multiple ferredoxin isoforms in Chlamydomonas reinhardtii - their role under stress conditions and biotechnological implications. Eur. J. Cell Biol. 89, 998-1004.
78. Xu, C., Moellering, E.R., Muthan, B., Fan, J. and Benning, C. (2010) Lipid transport mediated by Arabidopsis TGD proteins is unidirectional from the endoplasmic reticulum to the plastid. Plant Cell Physiol. 51, 1019-1028.
79. Zhang, Y., Adams, I.P. and Ratledge, C. (2007) Malic enzyme: the controlling activity for lipid production? Overexpression of malic enzyme in Mucor circinelloides leads to a 2.5-fold increase in lipid accumulation. Microbiology, 153, 2013-2025.