Photosynthetic carbon metabolism and biochemical composition of spring phytoplankton assemblages enclosed in microcosms: the diatom - Phaeocystis sp. succession

Samples of natural phytoplankton assemblages were taken on 4 occasions between 28 March and 19 April 1990 at 2 stations located to the southwest of Plymouth (UK) and incubated in experimental microcosms under constant light and temperature. 14C incorporation into cell constituents [proteins, polysaccharides, lipids and low molecular weight metabolites (LMWM)] and the biochemical compos~tion of the phytoplankton were monitored during the experiments. Different phytoplankton populations developed in the microcosms. Microflagellates which dominated in the f~rst experiments were followed in later experiments by a multispecific bloom of chain-forming diatoms, and these in turn by a bloom of Phaeocystis sp. Each assemblage was characterized by a different metabolic behaviour High '"C incorporation into LMWM and lip~ds was observed during non-growth periods when microflagellates dominated. High '"C incorporation into proteins and relatively high specific rates of protein synthesis (0.45 f 0.1 d-l) were measured during the late growth phase of the diatom bloom. Synthesis of acid-soluble carbohydrates (ASC) also occurred in this period. As Phaeocystis sp. increased. I4C incorporation into LMWM and polysaccharides showed a significant rise. These metabolic patterns were consistent with earlier models of the development of Phaeocystis sp. blooms. Polysaccharidecarbon concentration, both acid-soluble and acid-insoluble, showed dramatic increases during the early stages of the bloom. Enhanced polysaccharide synthesis was related to the formation of the mucilaginous colonial matrix and is suggested to be a physiological strategy tending to increase colony buoyancy. During the decline of the Phaeocystjs sp. bloom, the proportion of 14C incorporated into LMWM decreased, possibly as a result of disruption of the colonies, whereas incorporation into lipids exhibited a consistent increase. The accumulation of high-energy storage products is interpreted as a metabolic adaptation for overwintering under very low light levels. As a consequence of the distinct metabolic patterns of each successional stage, the protein-C/acid-insoluble polysaccharide-C ratio showed a marked decrease, whereas the relative contribution of ASC-C to the total measured carbon displayed a significant increase. In addition, carbon incorporation into LMWM also showed a slight but continuous increase. It is suggested that the metabolic changes associated with the diatom -Phaeocystis sp. succession are in accord with a marked shift in the trophic structure of the planktonic ecosystem from the classical food chain in the earlier stages, and mainly during the diatom bloom, to a preponderance of the microbial loop at the end of the Phaeocystis sp. bloom INTRODUCTION physiological adaptation involves a complex series of interacting processes, occurring on different time Phytoplankton cells have the capacity to rapidly scales which ultimately define the physiological state adjust their photosynthetic metabolism in response to and, consequently, the growth rate of a given populachanges in their physico-chemical environment. Their tion. Knowledge of these processes is central to the O Inter-Research 1992 90 Mar. Ecol. Prog. Ser. 90: 89-102, 1992 understanding of the physiological strategies adopted by phytoplankton and how these influence species succession. One of the frequently employed approaches dealing with this topic 1s to study the patterns of synthesis of organic polymers through examlnlng I4C labell~ng of the primary cellular biochemical pools (i.e. proteins, carbohydrates and lipids) (see review in Morris 1981). The main interest of this approach lies, firstly, in the recognized strong correlation between protein synthesis and population growth rate as revealed in culture work and field studies of both freshwater and marine systems (Morris et al. 1974, Lancelot et al. 1986, Lean et al. 1989), and, secondly, in the close relationship frequently found between photosynthate partitioning and phytoplankton physiological state (Morris 1981, Barlow 1984, Hama & Honjo 1987). Furthermore, the relative rates of synthesis of the major cellular bionioiecuieb will partially determine the chemical composition of the population. Extensive culture work has been carried out to clarify the influence that diverse environmental factors such as tcmperature, irradiance, the spectral quality of the light and inorganic nutrient concentration exert upon the flows of newly incorporated photosynthetic carbon in isolated phytoplankton species (e.g. Morris et al. 1974, Konopka 1983, Harding et al. 1985, Rivkin 1989). Most of these studies employed the solvent extraction protocol described by Li et al. (1980). In spite of the methodological limitations reported for this method (McConville et al. 1985, Hama et al. 1988b), some general patterns at the cellular level have emerged; most of the results obtained in these investigations cannot, however, be extrapolated easily to natural conditions. Changes in carbon metabolism observed in multispecific natural phytoplankton assemblages in response to the environment reflect a combination of within-species physiological adaptations superimposed upon changes in species composition. Given that both processes, although occurring simultaneously, operate on different time scales, and because ~ntclrspecific differences in photosynthetic carbon incorporation have been shown to be significant (Rivkin 1985, Madariaga 1992), the determination and interpretation of phytoplankton physiological state at the community level are extreme1.y difficult The sampling and experimental design undertaken in this study represent attempts to overcome some of these problems by examining the changes in physiological state and the subsequent modifications in biochemical composition of natural phytoplankton popula t ion~ on 2 different tim.e scales Firstly, short-term vanations within a population were deter:mined by monitoring the labelling patterns of assimilated carbon in natural assemblages contained In experimental microcosms at 12 h intervals. Secondly, mesoscale metabolic changes at the community level were examined in this work by repeating the same experimental procedure throughout early spring During this period, phytoplankton assemblages in temperate coastal areas undergo major changes in species composition from chain-forming diatoms to the colonial prymnesiophyte Phaeocystis sp. (Holligan & Harbour 1977, Lancelot & Mathot 1987). As far as we are aware, there are no published data linking daily patterns of photosynthetic carbon metabolism to the resulting biochemical composition, at both population and successional levels, during the highly variable mixed-stratified transition period in temperate seas. The experimental study ran in parallel with a spring bloom field survey (Davies et al. 1992), in order to determine the changes in carbon flows into photosyfithctic end-products and biochemics! composition associated with the growth and decline phases of the phytoplankton during the diatom Phaeocystis sp. succession.