Effect of growth rate and CO , concentration on carbon isotopic fractionation by the marine diatom Phaeodactylum tricornutum

Content Provider	Semantic Scholar
Author	Laws, Edward A. Bidigare, Robert R. Popp, Brian N.
Copyright Year	1999
Abstract	The carbon isotopic composition (813C) of the marine diatom PhaeodactylurY1 tricomutum was measured over a series of growth rates (p) in a chemostat system in which both the Si3C and the concentration of aqueous CO, [CO,(aq)] were measured. CO,(aq) ranged from 0.64 to 35 pmol kg-l and growth rates from 0.5 to 1.4 d-l. eP, the biological fractionation factor associated with carbon fixation, was found to bc a nonlinear function of @O,(aq), contrary to the predictions of a model that assumes that CO, enters the cell by passive diffusion. The experimental results suggest that active uptake of bicarbonate does not account for the nonlinearity of the relationship and that inorganic carbon enters the cell as CO,. The data are very well described by a theoretical model that assumes that P. tricornutum regulates the CO, concentration in its cytoplasm so as to minimize the energy required to concentrate CO, at the site of carboxylation. This is probably achieved by active uptake of CO, or by conversion of bicarbonate to CO, by an external carbonic anhydrase followed by transport of the CO, into the cell via either active transport or passive diffusion. Based on the model and data, @ZO,(aq) = 0.225 X [(26.8 a)/(~, 5.5)] kg d-’ pmol-l. This equation accounts for 92% of the variance in the @ZO,(aq) data. The model has potential utility for estimating phytoplankton growth rates in field studies without incubations and has important implications for the estimation of ancient CO,(aq) from the 613C of preserved organic compounds. There is general agreement that the 13C : 12C ratio of the organic carbon in plants reflects both the physiological condition of the plants and certain aspects of the environment at the time the organic matter was formed. Farquhar et al. (1982), for example, demonstrated that the combined effects of diffusion of CO, into a plant and isotopic discrimination by the primary carboxylating enzyme ribulose bisphosphate carboxylase oxygenase (Rubisco) would lead to approximately a linear relationship between the 613C of plant organic matter and the ration of the internal-to-external CO, concentrations. Fry and Wainright (1991) first recognized that both aqueous CO, concentrations and microalgal growth rates would influence the 613C of phytoplankton, and Rau et al. (1992) pointed out that negative correlations between the S”C of suspended particulate organic matter and concentrations of aqueous CO, could be explained by variations in phytoplankton demand for CO,. Francois et al. (1993) showed that if passive diffusion dominated carbon transport into phytoplankton cells, there should exist a linear relationship between the ST of phytoplankton organic carbon and the ratio of the carboxylation rate to external aqueous CO, concentration. Building on this earlier work, Goericke et al. (I 994) and Laws et al. (1995) derived equations that predicted that the S’“C of microalgal organic carbon should be Acknowledgments This work was supported by National Science Foundation grant OCE 93-01204. We gratefully acknowledge the technical assistance of David Hashimoto and Stephanie Christensen. This paper is SOEST contribution 4561. approximately a linear function of the ratio of the microalgal growth rate (p) to the aqueous CO, concentration as long as the movement of CO, into the cell was controlled by diffusion. Although the biochemical characteristics of phytoplankton are in many respects similar to those of conventional C, higher plants (K.erby and Raven 1985), some of their gas exchange characteristics more closely resemble those of C, plants. Phytoplankton have high affinities for CO,, low levels of inhibition of photosynthesis by oxygen, and low CO, compensation concentrations (Burns and Beardall 1987). These characteristics have suggested that they may possess a CO,-concentraing mechanism (CCM), which increases the CO, concentration at the active site of Rubisco. The existence of a CCM in marine microalgae has been inferred from the fact that at 1ow external CO, or inorganic carbon concentrations, the corresponding intracellular concentrations exceed the concentrations in the growth medium (Zenvirth and Kaplan 1911; Badger and Andrews 1982; Burns and Beardall 1987). 1Jncertainty regarding the nature of the CCM concerns (1) whether inorganic carbon is actively transported into the cell and if so whether bicarbonate or CO, is actively transported, (2) whether the CCM is located at the chloroplast envelope or at the plasmalemma, and (3) whether carbonic anhydrase (CA) is associated with the CCM and if so whether it is internal or external (Burns and Beardall 1987). The existence of a CCM and the possible use of bicarbonate as a sour-ce of inorganic carbon have important implications for the interpretation of 613C values in microalgae. If inorganic carbon enters the cell primarily by active trans-
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