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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.

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 huxleyiandCalcidiscus 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.