Modelling the pyrenoid-based CO₂-concentrating mechanism provides insights into its operating principles and a roadmap for its engineering into crops

TY - JOUR

T1 - Modelling the pyrenoid-based CO2-concentrating mechanism provides insights into its operating principles and a roadmap for its engineering into crops

AU - Fei, Chenyi

AU - Wilson, Alexandra T.

AU - Mangan, Niall M.

AU - Wingreen, Ned S.

AU - Jonikas, Martin C.

N1 - Publisher Copyright: © 2022, The Author(s).

PY - 2022/5

Y1 - 2022/5

N2 - Many eukaryotic photosynthetic organisms enhance their carbon uptake by supplying concentrated CO2 to the CO2-fixing enzyme Rubisco in an organelle called the pyrenoid. Ongoing efforts seek to engineer this pyrenoid-based CO2-concentrating mechanism (PCCM) into crops to increase yields. Here we develop a computational model for a PCCM on the basis of the postulated mechanism in the green alga Chlamydomonas reinhardtii. Our model recapitulates all Chlamydomonas PCCM-deficient mutant phenotypes and yields general biophysical principles underlying the PCCM. We show that an effective and energetically efficient PCCM requires a physical barrier to reduce pyrenoid CO2 leakage, as well as proper enzyme localization to reduce futile cycling between CO2 and HCO3−. Importantly, our model demonstrates the feasibility of a purely passive CO2 uptake strategy at air-level CO2, while active HCO3− uptake proves advantageous at lower CO2 levels. We propose a four-step engineering path to increase the rate of CO2 fixation in the plant chloroplast up to threefold at a theoretical cost of only 1.3 ATP per CO2 fixed, thereby offering a framework to guide the engineering of a PCCM into land plants.

AB - Many eukaryotic photosynthetic organisms enhance their carbon uptake by supplying concentrated CO2 to the CO2-fixing enzyme Rubisco in an organelle called the pyrenoid. Ongoing efforts seek to engineer this pyrenoid-based CO2-concentrating mechanism (PCCM) into crops to increase yields. Here we develop a computational model for a PCCM on the basis of the postulated mechanism in the green alga Chlamydomonas reinhardtii. Our model recapitulates all Chlamydomonas PCCM-deficient mutant phenotypes and yields general biophysical principles underlying the PCCM. We show that an effective and energetically efficient PCCM requires a physical barrier to reduce pyrenoid CO2 leakage, as well as proper enzyme localization to reduce futile cycling between CO2 and HCO3−. Importantly, our model demonstrates the feasibility of a purely passive CO2 uptake strategy at air-level CO2, while active HCO3− uptake proves advantageous at lower CO2 levels. We propose a four-step engineering path to increase the rate of CO2 fixation in the plant chloroplast up to threefold at a theoretical cost of only 1.3 ATP per CO2 fixed, thereby offering a framework to guide the engineering of a PCCM into land plants.

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U2 - 10.1038/s41477-022-01153-7

DO - 10.1038/s41477-022-01153-7

M3 - Article

C2 - 35596080

SN - 2055-026X

VL - 8

SP - 583

EP - 595

JO - Nature Plants

JF - Nature Plants

IS - 5

ER -