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Chloroplast and Mitochondria interactions for microalgal acclimation

Periodic Reporting for period 2 - ChloroMito (Chloroplast and Mitochondria interactions for microalgal acclimation)

Reporting period: 2021-07-01 to 2022-12-31

Photosynthesis emerged as an energy extraction process at least 3.5 billion years ago, first in anoxygenic bacteria and then in oxygen-producing organisms, leading to the evolution of complex life forms with an oxygen-based metabolism (such as humans). Oxygenic photosynthesis produces ATP and NADPH, and the right balance between these energy-rich molecules allows the assimilation of CO2 into organic matter. Although the mechanisms of ATP/NADPH synthesis are well understood, less is known about how CO2 assimilation was optimised. This process was essential for the successful phototrophic colonisation of land (by Plantae) and oceans (by phytoplankton). Plants and phytoplankton are known to adopt different acclimatisation strategies to ensure high efficiency photosynthesis under a wide range of environmental conditions. The different responses are probably the result of the different evolutionary origins of plastids. The emergence of photosynthetic cells by primary or secondary endosymbiosis involved not only the transfer of DNA from the symbiont to the host genome, but also the establishment of metabolic interactions between the symbiont and the host. This was a major challenge, as it involved the integration of a 'solar panel' (the future plastid) into a host cell that already had a 'petrol’ powered engine (the mitochondrion). The presence of the two engines posed a ‘plumbing’ problem for the host: how to connect the two devices. In the primary chloroplasts, present in Plantae, the connection was made at the level of metabolites. Genomic analysis of the first emerging primary endosymbionts suggests that pathogens (Chlamydia-like bacteria) donated genes to the host to facilitate the export of photosynthetic products from the chloroplast to the cytosol, where they are transformed into polysaccharides to fuel mitochondrial respiration. This solution allowed the energy autonomy of both organelles to be maintained. A different solution seems to have been adopted by the secondary endosymbiotic micro-organisms that colonised the oceans. In diatoms, ecologically efficient oceanic organisms, the chloroplast is directly connected to the mitochondria, promoting chloroplast-mitochondria exchanges, which optimise the distribution of ATP and NADPH to cellular functions during the day (when both engines are working) and at night (when only the mitochondria are functional). Is this second mechanism a paradigm for the optimisation of photosynthesis in the ocean? This is the main question ChloroMito is answering addressing the following objectives through a combination of genetics, cell tomography and single-cell spectroscopy approaches:
- What molecular mechanism(s) allow energy exchange between the two organelles?
- Are these mechanisms widely conserved in other oceanic taxa?
- Is this the solution adapted by phytoplankton to optimise their growth?
- Does it modulate the dynamic responses of phytoplankton to different integrated growth environments?

Overall, ChloroMito will change our understanding of oceanic photosynthesis, challenging concepts that are often deduced from plant-based concepts. This project will also generate new technologies suitable for the study of paradigm questions in photosynthesis beyond ChloroMito itself
The main scientific and technical achievements of ChloroMito in the different WPs include: i. the establishment of stable cultures of seven different eukaryotic microalgae, representing the main oceanic and/or laboratory model phytoplankton lineages. ii. Analysing them using focused ion beam scanning electron microscopy (FIB-SEM) to calculate the volume occupancy of major organelles and the volumetric ratios between plastids and mitochondria. These results lead to the hypothesis that the subcellular topology of phytoplankton is modulated by energy management constraints (Uwizeye et al, Nat commun 2021 and PNAS 2021). iii. assess the conservation of energy interactions between chloroplasts and mitochondria in these lines (Uwizeye et al, Nat Commun 2021), during acclimation to different growth conditions: light intensities (Uwizeye et al Nat Commun 2021) photosymbiosis (Uwizeye et al PNAS 2021) and trophic conditions (Curien et al, New Phytol 2021. Dal Bo et al, Front Plant Sci 2021; Uwizeye et al, Nat Commun 2021). Finally, iv. we tested the role of Phatr3_J39274, an ion transporter (KEA3), in the regulation of proton motive force (energy storage) in plastids. Loss of KEA3 alters the relationship between photosynthetic electron transfer (PET) and proton motive force (PMF), as well as responses to non-photochemical quenching (NPQ: thermal dissipation of excess absorbed light). We propose that KEA3 provides the bioenergetics flexibility required for diatom to thrive in different oceanic provinces (Seydoux, Storti et al, The New Phytol 2022).
Like all biological processes, photosynthesis is very sensitive to environmental fluctuations. The consequences of nutrient deprivation on photosynthetic CO2 uptake have been extensively studied: light can be a limiting substrate for photosynthesis, but it is often dissipated as heat in the ocean due to limited nutrient availability. Temperature affects nutrient availability by modulating the stratification of the ocean, resulting in different amounts of nutrients being available in the lower and upper layers of the water column. Despite the wealth of information on individual responses to stress, little is known about how photosynthetic marine organisms respond to changes in their environment as a whole. This knowledge will contribute significantly to our understanding of marine ecosystems and to predicting the ecological impact of climate change and human activities on these ecosystems. Previous studies on prokaryotes have led to the idea that phytoplankton respond primarily to global environmental challenges (the so-called "integrated growth environment") by appropriately allocating energy-rich resources (ATP and NADPH) to three main cellular sinks: CO2 assimilation, biosynthetic processes and cell division. Until the beginning of ChloroMito, no clear information was available on planktonic eukaryotes, despite their important position in the phytoplankton community.
The results published in Uwizeye et al. Nat Commun 2021 (phytoplankton subcellular architectures are modulated by energy management constraints) represent a major step in this direction. The discovery that environmental acclimation (the transition of the diatom Phaeodactylum from dim to bright light or the acclimation of Nannochloropsis to different trophic lifestyles) modulates cell volume occupancy by mitochondria and the plastid CO2-fixing compartment, while maintaining contacts between plastid mitochondria, provides the first pictures of phytoplankton acclimation at the cellular/subcellular level.
In the future, ChloroMito will continue to explore the structural/energetic constraint of phytoplankton acclimation, by combining cell biology/3D imaging (to decipher phytoplankton responses at subcellular scales), molecular biology (to identify the molecular actors of this subcellular energy exchange), biophysics (to validate these molecular actors by time-resolved spectroscopy) and ecophysiology (to compare the responses of evolutionarily distant phytoplankton taxa to environmental changes mimicking possible future ocean scenarios).