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J. Biol. Chem., Vol. 282, Issue 35, 25475-25486, August 31, 2007

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Anaerobic Acclimation in Chlamydomonas reinhardtii

ANOXIC GENE EXPRESSION, HYDROGENASE INDUCTION, AND METABOLIC PATHWAYS^*

Florence Mus¹, Alexandra Dubini^¶1, Michael Seibert¹, Matthew C. Posewitz^¶1, and Arthur R. Grossman¹²

From the Department of Plant Biology, Carnegie Institution, Stanford, California 94305, National Renewable Energy Laboratory, Golden, Colorado 80401, and ^¶Colorado School of Mines, Environmental Science and Engineering Division, Golden, Colorado 80401

Both prokaryotic and eukaryotic photosynthetic microbes experience conditions of anoxia, especially during the night when photosynthetic activity ceases. In Chlamydomonas reinhardtii, dark anoxia is characterized by the activation of an extensive set of fermentation pathways that act in concert to provide cellular energy, while limiting the accumulation of potentially toxic fermentative products. Metabolite analyses, quantitative PCR, and high density Chlamydomonas DNA microarrays were used to monitor changes in metabolite accumulation and gene expression during acclimation of the cells to anoxia. Elevated levels of transcripts encoding proteins associated with the production of H₂, organic acids, and ethanol were observed in congruence with the accumulation of fermentation products. The levels of over 500 transcripts increased significantly during acclimation of the cells to anoxic conditions. Among these were transcripts encoding transcription/translation regulators, prolyl hydroxylases, hybrid cluster proteins, proteases, transhydrogenase, catalase, and several putative proteins of unknown function. Overall, this study uses metabolite, genomic, and transcriptome data to provide genome-wide insights into the regulation of the complex metabolic networks utilized by Chlamydomonas under the anaerobic conditions associated with H₂ production.

Received for publication, February 16, 2007 , and in revised form, April 13, 2007.

^* This work was supported in part by National Science Foundation Grant MCB 0235878 (to A. R. G.), Air Force Office of Scientific Research Grant FA9550-05-1-0365 (to M. C. P.), and by the National Renewable Energy Laboratory, Laboratory Directed Research and Development Program (to M. S.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Tables I and II and Fig. 1.

¹ Supported by the Office of Biological and Environmental Research, Office of Science, United States Department of Energy.

² To whom correspondence should be addressed. Tel.: 650-325-1521 (Ext. 212); Fax: 650-325-6857; E-mail: arthurg{at}stanford.edu.

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