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Published on 17 May 2019
A major challenge for photosynthetic organisms is to efficiently acclimate to the highly dynamic light and nutrient conditions that occur to their natural environments. Yet, the molecular mechanisms controlling acclimation of microalgae to changing light and nutrient availability remain largely unknown. Our research aims to fill this gap of knowledge using mainly the model green microalga Chlamydomonas reinhardtii.

Current knowledge Light has two roles for photosynthetic organisms: sensed by photoreceptors it provides spatiotemporal information; absorbed by chloroplast pigments it supplies energy for photosynthesis (1). To thrive, plants and algae evolved the ability to integrate these two functions, through complex mechanisms currently not well understood. A main goal is to prevent lethal photodamage caused by excess light and they do so mainly via the photoprotection mechanism qE (energy quenching) (2).

Mutants of plants and algae with reduced qE have a strong fitness disadvantage (3-6). The importance of qE is also reflected by its regulatory complexity in the green microalga Chlamydomonas reinhardtii. In Chlamydomonas qE mainly depends on the nucleus-encoded, chloroplast-localized proteins LHCSR (LHCSR1 and LHCSR3), which are found in many algae and lower plants such as moss (4, 7). These proteins belong to the Light Harvesting Complex-Stress Related family (1). LHCSR3 is the main qE effector protein in high-light (4), although LHCSR1 can significantly contribute to qE under certain conditions (8). The transcriptional regulation of the LHCSR3 represents a perfect case study of cell signaling biology. Activation of LHCSR3 gene requires the absorption of blue-light by the photoreceptor phototropin (5) via the putative E3 ubiquitin ligase CUL4–DDB1DET1 (9) while it also involves calcium ion signalling and active photosynthetic electron transport (6) as well as a tightly controlled methylation of cytosine to 5-methylcytosine of the promoter region of the gene (18).

Environmental nutrient levels can vary from extreme excess to near total depletion. Suboptimal nutrient levels can cause slow plant growth and reduced biomass, while an excess of certain nutrients can stimulate algal blooms and eutrophication of aqueous habitats, impacting both biodiversity and ecosystem function at the global level (10). Similarly, the concentration of inorganic carbon (HCO3−, CO2 and CO32−, i.e. Ci) in aquatic environments is spatially and temporally variable and CO2, the substrate used for the fixation of Ci by photosynthesis, can be extremely abundant (oversaturated) or scarce (11). Under low Ci conditions, Chlamydomonas (and most other algae) elevates the CO2 concentration around the chloroplast-localized carboxylating enzyme RuBisCO (catalyzes initial reaction of CO2 fixation) by activating a cellular Ci concentrating mechanism (CCM) comprised of many proteins including carbonic anhydrases, which interconverts all forms of Ci, and high affinity transporters that bring Ci into the cell (12).

Nutrient and carbon limitations not only trigger a cellular metabolic readjustment but also impact the qE capacity of Chlamydomonas. Indeed, besides HL, LHCSR accumulation can be elicited by exposure to low Ci (13) as well as sulfur, nitrogen, phosphate) and iron (14-16) deprivation. On the other hand, excess Ci suppresses LHCSR3 without impacting expression of LHCSR1 (17).

Research questions
Overall, aim of our research is to mechanistically associate biological processes of fundamental importance for the biosphere, previously thought to be unrelated, i.e. photoperception, photoprotection, carbon and nutrient metabolism, by combining genetic, biochemical, molecular, physiological and mathematical modelling approaches. How do light and metabolic signals control gene expression in photosynthetic algae? What are the key molecular actors (genes, transcription factors, proteins, metabolites) for the processes of photoprotection and carbon metabolism? Our long-term vision is to obtain a systems view of cellular dynamics in photosynthetic microalgae.

We are currently addressing the following questions
1. What are the molecular actors controlling expression of LHCSR and CCM genes?
2. What is the mechanism of inhibition of gene expression of LHCSR and CCM genes by acetate and CO2?
3. How does PHOTOTROPIN, a blue light photoreceptor, transform light into biological signals in green algae?
4. How light quality impacts gene expression and carbon partitioning?

Cited references
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2. Li Z, Wakao S, Fischer BB and Niyogi KK. Sensing and responding to excess light. Annu. Rev. Plant Biol. 60, 239–260 (2009).
3. Külheim C, Agren J and Jansson S. Rapid regulation of light harvesting and plant fitness in the field. Science 297, 91–93 (2002).
4. Peers G et al. An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462, 518–521 (2009).
5. Petroutsos D et al. A blue-light photoreceptor mediates the feedback regulation of photosynthesis. Nature 537, 563–566 (2016).
6. Petroutsos D et al. The chloroplast calcium sensor CAS is required for photoacclimation in Chlamydomonas reinhardtii. Plant Cell 23, 2950–2963 (2011).
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14. Zhang Z et al. Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3, 1331–1348 (2004).
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18. Xue JH, Chen GD, Hao F, Chen H, Fang Z, Chen FF, Pang B, Yang QL, Wei X, Fan QQ et al. A Vitamin-C-derived DNA modification catalysed by an algal TET homologue. Nature, 14, 341 (2019).