Microalgae and cyanobacteria contribute roughly half of the global photosynthetic carbon assimilation. Faced with limited access to CO2in aquatic environments, which can vary daily or hourly, these microorganisms have evolved use of an efficient CO2concentrating mechanism (CCM) to accumulate high internal concentrations of inorganic carbon (Ci) to maintain photosynthetic performance. For eukaryotic algae, a combination of molecular, genetic and physiological studies using the model organism
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 diatom
- Award ID(s):
- 1744645
- NSF-PAR ID:
- 10400678
- Publisher / Repository:
- Springer Science + Business Media
- Date Published:
- Journal Name:
- Photosynthesis Research
- Volume:
- 156
- Issue:
- 2
- ISSN:
- 0166-8595
- Page Range / eLocation ID:
- p. 205-215
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Chlamydomonas reinhardtii , have revealed the function and molecular characteristics of many CCM components, including active Ciuptake systems. Fundamental to eukaryotic Ciuptake systems are Citransporters/channels located in membranes of various cell compartments, which together facilitate the movement of Cifrom the environment into the chloroplast, where primary CO2assimilation occurs. Two putative plasma membrane Citransporters, HLA3 and LCI1, are reportedly involved in active Ciuptake. Based on previous studies, HLA3 clearly plays a meaningful role in HCO3−transport, but the function of LCI1 has not yet been thoroughly investigated so remains somewhat obscure. Here we report a crystal structure of the full‐length LCI1 membrane protein to reveal LCI1 structural characteristics, as well asin vivo physiological studies in an LCI1 loss‐of‐function mutant to reveal the Cispecies preference for LCI1. Together, these new studies demonstrate LCI1 plays an important role in active CO2uptake and that LCI1 likely functions as a plasma membrane CO2channel, possibly a gated channel. -
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 alga
Chlamydomonas reinhardtii . Our model recapitulates allChlamydomonas 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 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. -
Membrane permeabilities to CO2and HCO3−constrain the function of CO2concentrating mechanisms that algae use to supply inorganic carbon for photosynthesis. In diatoms and green algae, plasma membranes are moderately to highly permeable to CO2but effectively impermeable to HCO3−. Here, CO2and HCO3−membrane permeabilities were measured using an18O‐exchange technique on two species of haptophyte algae,
Emiliania huxleyi andCalcidiscus leptoporus , which showed that the plasma membranes of these species are also highly permeable to CO2(0.006–0.02 cm · s−1) but minimally permeable to HCO3−. Increased temperature and CO2generally increased CO2membrane permeabilities in both species, possibly due to changes in lipid composition or CO2channel proteins. Changes in CO2membrane permeabilities showed no association with the density of calcium carbonate coccoliths surrounding the cell, which could potentially impede passage of compounds. Haptophyte plasma‐membrane permeabilities to CO2were somewhat lower than those of diatoms but generally higher than membrane permeabilities of green algae. One caveat of these measurements is that the model used to interpret18O‐exchange data assumes that carbonic anhydrase, which catalyzes18O‐exchange, is homogeneously distributed in the cell. The implications of this assumption were tested using a two‐compartment model with an inhomogeneous distribution of carbonic anhydrase to simulate18O‐exchange data and then inferring plasma‐membrane CO2permeabilities from the simulated data. This analysis showed that the inferred plasma‐membrane CO2permeabilities are minimal estimates but should be quite accurate under most conditions. -
Summary In response to high CO2environmental variability, green algae, such as
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