INAUGURAL ARTICLE by a Recently Elected Academy Member:Efficiency of the CO2-concentrating mechanism of diatoms

Diatoms evolved during the Mesozoic era and have gradually become major actors in the oceanic cycles of elements (1). Their precipitation of siliceous frustules now dominates the reverse weathering of silica, and their photosynthetic activity contributes some 40% of modern-day oceanic primary production. Because of their large size and silica ballast, they contribute a major fraction of the downward flux of particulate organic carbon and thus, a major fraction of the export of CO2 to deep seawater. The low modern-day CO2 concentration in surface seawater and the atmosphere that results from this biological carbon pump poses a challenge to photosynthetic organisms, including diatoms themselves. Like most photosynthetic organisms, they fix carbon using RubisCO as the carboxylating enzyme. Diatom RubisCOs suffer from the same slow turnover rate and wasteful tendency to fix O2 as other RubisCOs, and their affinity for CO2 is only marginally better (2, 3). As in other photosynthetic organisms, the main adaptation of diatoms to the gradual decrease in ambient CO2 and increase in O2 over geological times has been the evolution of a CO2 concentrating mechanism (CCM) to elevate the concentration of CO2 at the site of fixation by RubisCO (4–7). It is perhaps not an exaggeration to posit that today's atmospheric CO2 concentration is, in large part, determined by the efficiency of the CCM of diatoms. Despite its importance, the physiology/biochemistry of diatoms has been little studied compared with that of model photosynthetic organisms, and the CCM of diatoms is still poorly understood. Some species operate a C4-type pathway, whereas others seem to rely on active transport of HCO3− into the chloroplast (4–8). Active transport of inorganic carbon by the CCM is thought to account for a significant portion of cellular energy expenditure (2). Energy expenditure on the CCM is currently of interest, because savings from its down-regulation are likely to be responsible for the major acclimations of oceanic phytoplankton to rising CO2 over the next century. Because lipid bilayers are highly permeable to small uncharged molecules like CO2 (9), the CCM of unicellular organisms like diatoms is necessarily leaky; only a fraction of the CO2 molecules concentrated at the site of RubisCO end up being fixed, and the rest are lost by diffusion. The total energetic expenditure to operate a CCM is, thus, the product of the energy expended to concentrate 1 molecule CO2 at the site of fixation multiplied by the mole ratio of CO2 transported to CO2 fixed. However, at this point, neither of these terms is known with any precision. At the most basic level, we do not know how permeable to CO2 diatoms membranes really are and what barriers may slow down the outward diffusion of CO2 (10, 11). Here, we attempt a complete characterization of inorganic carbon fluxes in model diatoms using membrane inlet MS (MIMS) (12) and kinetic models of 18O isotope exchange from CO2.