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

Abstract

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 light-and 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...

von Liebig's law of the minimum and plankton ecology (1899–1991)

“…If that is true then CO 2 might become limiting for some species of algae (RAVEN and JOHNSTON, 1991). All reactions in the seawater CO 2 system (Fig.6) are very rapid, except the dissociation of riCO 3-to [CO2]aqeous (SKIRROW, 1975), which happens to be the one reaction the algae would have preferred to be fast.…”

Algal evolution in relation to atmospheric CO 2 : carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles

“…These characteristics would minimize the nitrogen needed to produce the machinery associated with a given rate of CO 2 fixation, and thus the phosphorus in RNA needed to synthesize the proteins [66]. Costs in energy, nitrogen, phosphorus, iron and manganese will be considered below in the context of decreasing CO 2 and increasing O 2 [66][67][68][69][70][71][72][73][74].…”

The development of a CO2‐concentrating mechanism in Emiliania huxleyi

“…investigated so far show the physiological characteristics of a DICconcentrating mechanism (Raven & Johnston, 1991) which allows these cells to carry out photosynthesis at optimal rates at very low ambient concentrations of CO,. In addition to the ability of cells to accumulate DIC internally to levels higher than could be obtained by simple diffusion (Badger et a!., 1980), the i?…”

“…The large intracellular inorganic carbon (Cj) concentration generated by the CCM decreases the oxygenase activity of Rubisco, so even at low external DIC concentration there is little inhibition of photosynthesis by oxygen, and a much * To whom correspondence should be addressed. reduced rate of photorespiration (Shelp & Canvin, 1980;Raven & Johnston, 1991). In addition, the cost efficiency of acquiring photons, nitrogen, iron, manganese and molybdenum to achieA'e a given rate of carbon accumulation in cells with a CCM might be better than in microalgae that rely on diffusive CO, entry (Raven, 1991;Raven & Johnston, 1991).…”

“…reduced rate of photorespiration (Shelp & Canvin, 1980;Raven & Johnston, 1991). In addition, the cost efficiency of acquiring photons, nitrogen, iron, manganese and molybdenum to achieA'e a given rate of carbon accumulation in cells with a CCM might be better than in microalgae that rely on diffusive CO, entry (Raven, 1991;Raven & Johnston, 1991). Some microalgai spp.…”