Abstract
The unicellular green alga Chlamydomonas reinhardtii is a long-established model organism for studies on photosynthesis and carbon metabolism-related physiology. Under conditions of air-level carbon dioxide concentration [CO2], a carbon concentrating mechanism (CCM) is induced to facilitate cellular carbon uptake. CCM increases the availability of carbon dioxide at the site of cellular carbon fixation. To improve our understanding of the transcriptional control of the CCM, we employed FAIRE-seq (formaldehyde-assisted Isolation of Regulatory Elements, followed by deep sequencing) to determine nucleosome-depleted chromatin regions of algal cells subjected to carbon deprivation. Our FAIRE data recapitulated the positions of known regulatory elements in the promoter of the periplasmic carbonic anhydrase (Cah1) gene, which is upregulated during CCM induction, and revealed new candidate regulatory elements at a genome-wide scale. In addition, time series expression patterns of 130 transcription factor (TF) and transcription regulator (TR) genes were obtained for cells cultured under photoautotrophic condition and subjected to a shift from high to low [CO2]. Groups of co-expressed genes were identified and a putative directed gene-regulatory network underlying the CCM was reconstructed from the gene expression data using the recently developed IOTA (inner composition alignment) method. Among the candidate regulatory genes, two members of the MYB-related TF family, Lcr1 (Low-CO 2 response regulator 1) and Lcr2 (Low-CO 2 response regulator 2), may play an important role in down-regulating the expression of a particular set of TF and TR genes in response to low [CO2]. The results obtained provide new insights into the transcriptional control of the CCM and revealed more than 60 new candidate regulatory genes. Deep sequencing of nucleosome-depleted genomic regions indicated the presence of new, previously unknown regulatory elements in the C. reinhardtii genome. Our work can serve as a basis for future functional studies of transcriptional regulator genes and genomic regulatory elements in Chlamydomonas.
Highlights
Like other green algae, Chlamydomonas reinhardtii has evolved an inorganic carbon (Ci) concentrating mechanism (CCM) to support photosynthetic carbon fixation
Studies on the cyanobacterium Synechocystis PCC6803 and the green alga Chlamydomonas acidophila have shown that cells cultivated at low-CO2 (LC) concentration in the light take up Ci more rapidly than cells cultivated at LC in the dark, suggesting a cooperative effect involving light and carbon signaling in the modulation of the expression of CCM-related genes [11,12]
Previous reports demonstrated enhanced expression of carbonic anhydrase1 (Cah1) and mitochondrial carbonic anhydrase (Mca) during CCM induction in Chlamydomonas wild-type strains cultured in photoautotrophic conditions [7,14]
Summary
Chlamydomonas reinhardtii has evolved an inorganic carbon (Ci) concentrating mechanism (CCM) to support photosynthetic carbon fixation. Through this mechanism, the availability of CO2 is increased in the vicinity of the carbon fixation enzyme, ribulose-1, 5 bisphosphate carboxylase oxygenase (Rubisco), favoring photosynthesis [1,2]. Studies on the cyanobacterium Synechocystis PCC6803 and the green alga Chlamydomonas acidophila have shown that cells cultivated at low-CO2 (LC) concentration in the light take up Ci more rapidly than cells cultivated at LC in the dark, suggesting a cooperative effect involving light and carbon signaling in the modulation of the expression of CCM-related genes [11,12]. The enzyme carbonic anhydrase equilibrates the cellular concentrations of CO2 and HCO3- and represents an important component of the CCM [1]; there is currently no complete understanding of the gene regulatory network underlying the CCM
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