Dramatic changes in mitochondrial subcellular location and morphology accompany activation of the CO ₂ concentrating mechanism

Journal Article · 15 October 2024 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.2407548121 · OSTI ID:2468728

Findinier, Justin  ^[1]; Joubert, Lydia-Marie  ^[2]; Fakhimi, Neda ^[1]; Schmid, Michael F.  ^[2]; Malkovskiy, Andrey V.  ^[1]; Chiu, Wah  ^[3]; Burlacot, Adrien ^[4]; Grossman, Arthur R.  ^[4]

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1. The Carnegie Institution for Science, Biosphere Sciences and Engineering, Stanford, CA 94305
2. SLAC National Accelerator Laboratory, Division of CryoElectron Microscopy and Bioimaging, Menlo Park, CA 94025
3. SLAC National Accelerator Laboratory, Division of CryoElectron Microscopy and Bioimaging, Menlo Park, CA 94025, Department of Bioengineering, Stanford University, Stanford, CA 94305
4. The Carnegie Institution for Science, Biosphere Sciences and Engineering, Stanford, CA 94305, Biology Department, Stanford University, Stanford, CA 94305

Dynamic changes in intracellular ultrastructure can be critical for the ability of organisms to acclimate to environmental conditions. Microalgae, which are responsible for ~50% of global photosynthesis, compartmentalize their Ribulose 1,5 Bisphosphate Carboxylase/Oxygenase (Rubisco) into a specialized structure known as the pyrenoid when the cells experience limiting CO ₂ conditions; this compartmentalization is a component of the CO ₂ Concentrating Mechanism (CCM), which facilitates photosynthetic CO ₂ fixation as environmental levels of inorganic carbon (Ci) decline. Changes in the spatial distribution of mitochondria in green algae have also been observed under CO ₂ limitation, although a role for this reorganization in CCM function remains unclear. We used the green microalga Chlamydomonas reinhardtii to monitor changes in mitochondrial position and ultrastructure as cells transition between high CO ₂ and Low/Very Low CO ₂ (LC/VLC). Upon transferring cells to VLC, the mitochondria move from a central to a peripheral cell location and orient in parallel tubular arrays that extend along the cell’s apico-basal axis. We show that these ultrastructural changes correlate with CCM induction and are regulated by the CCM master regulator CIA5. The apico-basal orientation of the mitochondrial membranes, but not the movement of the mitochondrion to the cell periphery, is dependent on microtubules and the MIRO1 protein, with the latter involved in membrane–microtubule interactions. Furthermore, blocking mitochondrial respiration in VLC-acclimated cells reduces the affinity of the cells for Ci. Overall, our results suggest that mitochondrial repositioning functions in integrating cellular architecture and energetics with CCM activities and invite further exploration of how intracellular architecture can impact fitness under dynamic environmental conditions.

• Sponsoring Organization: USDOE
• Grant/Contract Number: SC0019417
• OSTI ID: 2468728
• Journal Information: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 43 Vol. 121; ISSN 0027-8424
• Publisher: Proceedings of the National Academy of SciencesCopyright Statement
• Country of Publication: United States
• Language: English