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Abstract Marine diatoms are key primary producers across diverse habitats in the global ocean. Diatoms rely on a biophysical carbon concentrating mechanism (CCM) to supply high concentrations of CO2around their carboxylating enzyme, RuBisCO. The necessity and energetic cost of the CCM are likely to be highly sensitive to temperature, as temperature impacts CO2concentration, diffusivity, and the kinetics of CCM components. Here, we used membrane inlet mass spectrometry (MIMS) and modeling to capture temperature regulation of the CCM in the diatomPhaeodactylum tricornutum (Pt). We found that enhanced carbon fixation rates byPtat elevated temperatures were accompanied by increased CCM activity capable of maintaining RuBisCO close to CO2saturation but that the mechanism varied. At 10 and 18 °C, diffusion of CO2into the cell, driven byPt’s ‘chloroplast pump’ was the major inorganic carbon source. However, at 18 °C, upregulation of the chloroplast pump enhanced (while retaining the proportion of) both diffusive CO2and active HCO3−uptake into the cytosol, and significantly increased chloroplast HCO3−concentrations. In contrast, at 25 °C, compared to 18 °C, the chloroplast pump had only a slight increase in activity. While diffusive uptake of CO2into the cell remained constant, active HCO3−uptake across the cell membrane increased resulting inPtdepending equally on both CO2and HCO3−as inorganic carbon sources. Despite changes in the CCM, the overall rate of active carbon transport remained double that of carbon fixation across all temperatures tested. The implication of the energetic cost of thePtCCM in response to increasing temperatures was discussed.
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Modelling the pyrenoid-based CO2-concentrating mechanism provides insights into its operating principles and a roadmap for its engineering into crops
Abstract Many eukaryotic photosynthetic organisms enhance their carbon uptake by supplying concentrated CO2to 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 algaChlamydomonas reinhardtii. Our model recapitulates allChlamydomonasPCCM-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 CO2leakage, as well as proper enzyme localization to reduce futile cycling between CO2and HCO3−. Importantly, our model demonstrates the feasibility of a purely passive CO2uptake strategy at air-level CO2, while active HCO3−uptake proves advantageous at lower CO2levels. We propose a four-step engineering path to increase the rate of CO2fixation in the plant chloroplast up to threefold at a theoretical cost of only 1.3 ATP per CO2fixed, thereby offering a framework to guide the engineering of a PCCM into land plants.
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- Award ID(s):
- 1935444
- PAR ID:
- 10367294
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Plants
- Volume:
- 8
- Issue:
- 5
- ISSN:
- 2055-0278
- Page Range / eLocation ID:
- p. 583-595
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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