A promiscuous mechanism to phase separate eukaryotic carbon fixation in the green lineage

James Barrett; Mihris I S Naduthodi; Yuwei Mao; Clément Dégut; Sabina Musiał; Aidan Salter; Mark C Leake; Michael J Plevin; Alistair J McCormick; James N Blaza; Luke C M Mackinder

doi:10.1038/s41477-024-01812-x

A promiscuous mechanism to phase separate eukaryotic carbon fixation in the green lineage

James Barrett, Mihris I S Naduthodi, Yuwei Mao, Clément Dégut, Sabina Musiał, Aidan Salter, Mark C Leake, Michael J Plevin, Alistair J McCormick, James N Blaza, Luke C M Mackinder

Research output: Contribution to journal › Article › peer-review

Abstract

CO2 fixation is commonly limited by inefficiency of the CO2-fixing enzyme Rubisco. Eukaryotic algae concentrate and fix CO2 in phase-separated condensates called pyrenoids, which complete up to one-third of global CO2 fixation. Condensation of Rubisco in pyrenoids is dependent on interaction with disordered linker proteins that show little conservation between species. We developed a sequence-independent bioinformatic pipeline to identify linker proteins in green algae. We report the linker from Chlorella and demonstrate that it binds a conserved site on the Rubisco large subunit. We show that the Chlorella linker phase separates Chlamydomonas Rubisco and that despite their separation by ~800 million years of evolution, the Chlorella linker can support the formation of a functional pyrenoid in Chlamydomonas. This cross-species reactivity extends to plants, with the Chlorella linker able to drive condensation of some native plant Rubiscos in vitro and in planta. Our results represent an exciting frontier for pyrenoid engineering in plants, which is modelled to increase crop yields.

Original language	English
Number of pages	33
Journal	Nature Plant
Early online date	9 Oct 2024
DOIs	https://doi.org/10.1038/s41477-024-01812-x
Publication status	E-pub ahead of print - 9 Oct 2024

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10.1038/s41477-024-01812-xLicence: CC BY

A promiscuous mechanism to phase separate eukaryotic carbon fixation in the green lineage
© The Author(s) 2024
Final published version, 15.5 MBLicence: CC BY

Cite this

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title = "A promiscuous mechanism to phase separate eukaryotic carbon fixation in the green lineage",

abstract = "CO2 fixation is commonly limited by inefficiency of the CO2-fixing enzyme Rubisco. Eukaryotic algae concentrate and fix CO2 in phase-separated condensates called pyrenoids, which complete up to one-third of global CO2 fixation. Condensation of Rubisco in pyrenoids is dependent on interaction with disordered linker proteins that show little conservation between species. We developed a sequence-independent bioinformatic pipeline to identify linker proteins in green algae. We report the linker from Chlorella and demonstrate that it binds a conserved site on the Rubisco large subunit. We show that the Chlorella linker phase separates Chlamydomonas Rubisco and that despite their separation by ~800 million years of evolution, the Chlorella linker can support the formation of a functional pyrenoid in Chlamydomonas. This cross-species reactivity extends to plants, with the Chlorella linker able to drive condensation of some native plant Rubiscos in vitro and in planta. Our results represent an exciting frontier for pyrenoid engineering in plants, which is modelled to increase crop yields.",

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AU - Barrett, James

AU - Naduthodi, Mihris I S

AU - Mao, Yuwei

AU - Dégut, Clément

AU - Musiał, Sabina

AU - Salter, Aidan

AU - Leake, Mark C

AU - Plevin, Michael J

AU - McCormick, Alistair J

AU - Blaza, James N

AU - Mackinder, Luke C M

PY - 2024/10/9

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AB - CO2 fixation is commonly limited by inefficiency of the CO2-fixing enzyme Rubisco. Eukaryotic algae concentrate and fix CO2 in phase-separated condensates called pyrenoids, which complete up to one-third of global CO2 fixation. Condensation of Rubisco in pyrenoids is dependent on interaction with disordered linker proteins that show little conservation between species. We developed a sequence-independent bioinformatic pipeline to identify linker proteins in green algae. We report the linker from Chlorella and demonstrate that it binds a conserved site on the Rubisco large subunit. We show that the Chlorella linker phase separates Chlamydomonas Rubisco and that despite their separation by ~800 million years of evolution, the Chlorella linker can support the formation of a functional pyrenoid in Chlamydomonas. This cross-species reactivity extends to plants, with the Chlorella linker able to drive condensation of some native plant Rubiscos in vitro and in planta. Our results represent an exciting frontier for pyrenoid engineering in plants, which is modelled to increase crop yields.

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