Review: Algal pyrenoids in global carbon cycling: frontier research on structure, function, and convergent evolution

Abstract

Carbon dioxide (CO₂) fixation in aqueous environments presents a major challenge for photosynthetic organisms due to slow CO₂ diffusion rates and the low affinity of CO₂-fixing enzyme Rubisco for CO₂. Algae have evolved CO₂-concentrating mechanisms (CCMs) centered around a specialized non-membrane-bound organelle called the pyrenoid, which concentrates Rubisco through liquid-liquid phase separation. The pyrenoid architecture comprises three key features: a Rubisco-rich matrix formed through phase separation with the linker protein EPYC1, a surrounding starch sheath that acts as a CO₂ diffusion barrier, and specialized pyrenoid tubules that facilitate CO₂ delivery. Recent studies using the model green alga, Chlamydomonas reinhardtii, have revealed that pyrenoid assembly and maintenance are regulated by complex molecular mechanisms, including multivalent protein interactions, dynamic protein relocalization, and calcium-dependent signaling pathways. Environmental CO₂ levels trigger distinct carbon uptake pathways that are energized by photosynthetic and mitochondrial electron transport. Engineering efforts to introduce pyrenoid-based CCMs into crops have made significant progress, with successful reconstitution of matrix formation, starch recruitment, and thylakoid membrane extensions in plant chloroplasts. These advances provide new opportunities for improving crop photosynthetic efficiency while offering insights into phase separation-driven organelle assembly.