Photosynthetic carbon (C) fixation by phytoplankton in the Southern Ocean (SO) plays a critical role in regulating air–sea exchange of carbon dioxide and thus global climate. In the SO, photosynthesis (PS) is often constrained by low iron, low temperatures, and low but highly variable light intensities. Recently, proton-pumping rhodopsins (PPRs) were identified in marine phytoplankton, providing an alternate iron-free, light-driven source of cellular energy. These proteins pump protons across cellular membranes through light absorption by the chromophore retinal, and the resulting pH energy gradient can then be used for active membrane transport or for synthesis of adenosine triphosphate. Here, we show that PPR is pervasive in Antarctic phytoplankton, especially in iron-limited regions. In a model SO diatom, we found that it was localized to the vacuolar membrane, making the vacuole a putative alternative phototrophic organelle for light-driven production of cellular energy. Unlike photosynthetic C fixation, which decreases substantially at colder temperatures, the proton transport activity of PPR was unaffected by decreasing temperature. Cellular PPR levels in cultured SO diatoms increased with decreasing iron concentrations and energy production from PPR photochemistry could substantially augment that of PS, especially under high light intensities, where PS is often photoinhibited. PPR gene expression and high retinal concentrations in phytoplankton in SO waters support its widespread use in polar environments. PPRs are an important adaptation of SO phytoplankton to growth and survival in their cold, iron-limited, and variable light environment.
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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.