Global transcriptomic analysis of Cyanothece 51142 reveals robust diurnal oscillation of central metabolic processes

doi:10.1073/pnas.0711068105

Global transcriptomic analysis of Cyanothece 51142 reveals robust diurnal oscillation of central metabolic processes

*Department of Biology, Washington University, St. Louis, MO 63130; and
^†Department of Molecular Microbiology and Immunology, Saint Louis University School of Medicine, St. Louis, MO 63104

Edited by Robert Haselkorn, University of Chicago, Chicago, IL, and approved February 13, 2008 (received for review November 21, 2007)

Abstract

Cyanobacteria are photosynthetic organisms and are the only prokaryotes known to have a circadian lifestyle. Unicellular diazotrophic cyanobacteria such as Cyanothece sp. ATCC 51142 produce oxygen and can also fix atmospheric nitrogen, a process exquisitely sensitive to oxygen. To accommodate such antagonistic processes, the intracellular environment of Cyanothece oscillates between aerobic and anaerobic conditions during a day–night cycle. This is accomplished by temporal separation of the two processes: photosynthesis during the day and nitrogen fixation at night. Although previous studies have examined periodic changes in transcript levels for a limited number of genes in Cyanothece and other unicellular diazotrophic cyanobacteria, a comprehensive study of transcriptional activity in a nitrogen-fixing cyanobacterium is necessary to understand the impact of the temporal separation of photosynthesis and nitrogen fixation on global gene regulation and cellular metabolism. We have examined the expression patterns of nearly 5,000 genes in Cyanothece 51142 during two consecutive diurnal periods. Our analysis showed that ≈30% of these genes exhibited robust oscillating expression profiles. Interestingly, this set included genes for almost all central metabolic processes in Cyanothece 51142. A transcriptional network of all genes with significantly oscillating transcript levels revealed that the majority of genes encoding enzymes in numerous individual biochemical pathways, such as glycolysis, oxidative pentose phosphate pathway, and glycogen metabolism, were coregulated and maximally expressed at distinct phases during the diurnal cycle. These studies provide a comprehensive picture of how a physiologically relevant diurnal light–dark cycle influences the metabolism in a photosynthetic bacterium.

Footnotes

^‡To whom correspondence should be addressed. E-mail: pakrasi{at}wustl.edu
Author contributions: J.S., E.A.W., M.L., R.K., R.A., and H.B.P. designed research; J.S. and M.L. performed research; E.A.W., R.K., and R.A. contributed new reagents/analytic tools; J.S. and E.A.W. analyzed data; and J.S., E.A.W., and M.L. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The genome sequence reported in this paper has been deposited in the GenBank database (accession nos. CP000806–CP000811). The microarray data have been deposited in the European Bioinformatics Institute ArrayExpress database (accession nos. A-MEXP-864 and E-TABM-337).
This article contains supporting information online at www.pnas.org/cgi/content/full/0711068105/DCSupplemental.