Mechanisms of inorganic-carbon acquisition in marine phytoplankton and their implications for the use of other resources

Most of the marine phytoplankton species for which data are available are rate saturated for photosynthesis and probably for growth with inorganic C at normal seawater concentrations; 2 of the 17 species are not saturated. Photosynthesis in these two species can probably be explained by assuming that CO, reaches the site of its reaction with RUBISCO (ribulose bisphosphate carboxylase-oxygenase) by passive diffusion. The kinetics of CO, fixation by intact cells are explicable by RUBISCO kinetics typical of (eucaryotic) algae, and a CO,-saturated in vivo RUBISCO activity not more than twice the in vivo lightand inorganic-C-saturated rate of photosynthesis. For the other species, the high affinity in vivo for inorganic C (and several other attributes) could be explained by postulating active influx of inorganic C yielding a higher concentration of CO, available to RUBISCO during steady state photosynthesis than in the medium. Although such a higher concentration of internal CO, in cells with high affinity for inorganic C is found at low (subseawater) levels of external inorganic C, the situation is more equivocal at normal seawater concentrations. In theory, the occurrence of a CO,-concentrating mechanism rather than passive CO, entry (with consequent glycolate synthesis and metabolism or excretion) could reduce the photon, N, Fe, Mn, and MO costs of growth, but increase the Zn and Se costs. Thus far, data on costs are available only for photons and N; these data generally agree with the predicted lower costs for cells with high affinity for inorganic C. The ecological significance of these attributes is that most marine phytoplankters are not likely to have photosynthetic or growth rates reduced by the measured decreases in inorganic C in productive seawater, drawdown of inorganic C in productive seawater (or increase as atmospheric CO, increases) might alter the competitive balance between cells with low and high affinity for inorganic C, and differences in the effectiveness of use of other resources between cells with high and low affinity could cause differences in the rate and extent of resourcelimited growth for communities dominated by high-affinity or low-affinity cells. The influence of external inorganic-C concentration on growth and photosynthesis by marine phytoplankton organisms has been little investigated relative to the effects of concentrations of NH4+, N03-, urea, HP042-, and Si(OH),, or even the experimentally less tractable transition metals. The related phenomena of the small drawdown of inorganic-C levels in highly productive (N, P, Fe-rich) regions of the ocean and the (inferred) absence of growth limitation of marine phytoplankton by inorganic C can explain this relative neglect. However, the data discussed here (see Raven 199 la,b; Raven and Johnston in press) show that there are major differences between marine phytoplankton species with respect to inorganic-c affinity, that these differences could alter relative competitive abilities within the observed ranges of inorganic C at the ocean surface (e.g. Rau et al. 1989), and that the likely differences in mechanism between cells with high and low affinity for inorganic C could be associated with differences in the cost of photons, N, Fe, Mn, or MO for growth. Physiology of inorganic-C acquisition Table 1 shows values from the literature (and unpublished work on Phaeodactylum tricornutum) on the half-saturation values for acquisition of inorganic C in photosynthesis. The data can be divided into two groups, a large one with a K,,2 for CO2 of < 1.7 mmol ma3 ( 15 of 17 species), while the other organisms (Emiliania huxleyi, Stichococcus minor) have K, values for CO2 of 9.0 mmol me3. Objections can be raised as to the small number of species examined and the extent to which they are representative of oceanic phytoplankton, but the 17 species examined cover eight major taxa 1702 Raven and Johnston Table 1. K,/, values (mmol m-3) for inorganic C in marine phytoplankton photosynthesis, expressed in terms of free CO, and of HCO,-. All data for cells grown at air-equilibrium CO, levels; experiments conducted in seawater or artificial seawater at pH 7.5-8.0, temperature 18?-25°C; see original reference for specific details. Except for A. carterae, the first value for P. tricornutum, and A!?. huxleyi, for which inorganic 14C was used, all data relate to inorganic-C-dependent 0, evolution.