Pyrenoid-core CO2-evolving machinery is essential for diatom photosynthesis in elevated CO2

• Published in: Plant physiology (Bethesda) Vol. 193; no. 4; pp. 2298 - 2305
• Main Authors: Shimakawa, Ginga, Okuyama, Akane, Harada, Hisashi, Nakagaito, Shuko, Toyoshima, Yui, Nagata, Kazuya, Matsuda, Yusuke
• Format: Journal Article
• Language: English
• Published: US Oxford University Press 22.11.2023
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1093/plphys/kiad475

Abstract Marine diatoms are responsible for up to 20% of the annual global primary production by performing photosynthesis in seawater where CO2 availability is limited while HCO3− is abundant. Our previous studies have demonstrated that solute carrier 4 proteins at the plasma membrane of the diatom Phaeodactylum tricornutum facilitate the use of the abundant seawater HCO3−. There has been an unconcluded debate as to whether such HCO3− use capacity may itself supply enough dissolved inorganic carbon (DIC) to saturate the enzyme Rubisco. Here, we show that the θ-type carbonic anhydrase, Ptθ-CA1, a luminal factor of the pyrenoid-penetrating thylakoid membranes, plays an essential role in saturating photosynthesis of P. tricornutum. We isolated and analyzed genome-edited mutants of P. tricornutum defective in Ptθ-CA1. The mutants showed impaired growth in seawater aerated with a broad range of CO2 levels, from atmospheric to 1%. Independently of growth CO2 conditions, the photosynthetic affinity measured as K0.5 for DIC in mutants reached around 2 mm, which is about 10 times higher than K0.5[DIC] of high-CO2–grown wild-type cells that have repressed CO2-concentrating mechanism levels. The results clearly indicate that diatom photosynthesis is not saturated with either seawater-level DIC or even under a highly elevated CO2 environment unless the CO2-evolving machinery is at the core of the pyrenoid. CO2-evolving machinery in the pyrenoid-penetrating thylakoid membrane is critical to provide CO2 to condensed Rubisco, even in an elevated CO2 environment, in marine diatoms.