Trophic upgrading of autotrophic picoplankton by the heterotrophic nanoflagellate Paraphysomonas sp

We investigated whether trophic repackaging of autotrophic picoplankton by phagotrophic protists is associated with an improvement in food quality for the metazooplankton Daphnia magna (i.e., whether trophic upgrading occurs in this system). The nutritional value of the autotrophic species Microcystis aeruginosa PCC7806, Synechococcus sp. strain BO8809, Synechococcus elongatus SAG 89.79, and Choricystis minor KR1988/ 8, and of the heterotrophic nanoflagellate Paraphysomonas sp. grown on these different picoplanktonic species was evaluated in standardized growth experiments with D. magna. In order to investigate the functional role of the flagellate in the simplified autotrophic picoplankton–Daphnia food chain, Paraphysomonas sp. was grown on the different picoplanktonic organisms and subsequently separated from the food items before being fed to D. magna. The presence of Paraphysomonas sp. as an intermediary trophic step enhanced somatic growth and reproduction of D. magna. Supplementation of Synechococcus sp. with lipids from Paraphysomonas sp. (grown on Synechococcus sp.) revealed that trophic upgrading of autotrophic picoplankton is due to the additional lipids present in the flagellate. Paraphysomonas sp. synthesized polyunsaturated fatty acids and sterols de novo, which most likely explains the trophic upgrading. Paraphysomonas sp. also improved the food quality of M. aeruginosa PCC7806, which is toxic for D. magna. The heterotrophic flagellate Paraphysomonas sp. is capable of trophically upgrading a poor quality food source not only by producing essential lipids, but also by detoxifying the cyanobacterial food organism. The consumption of picoplanktonic organisms (heterotrophic bacteria and autotrophic picoplankton) by phagotrophic protists has been recognized as a major pathway of carbon flow (Azam et al. 1983). Autotrophic picoplankton (APP) accounts for the bulk of primary production in large parts of open oceans and in many oligotrophic lakes (Weisse 1993; Callieri and Stockner 2002). However, such picoplankton is largely unavailable to direct consumption by most crustacean grazers (except cladocerans), whose grazing apparatus is too coarse to retain picoplanktonic particles. In contrast, heterotrophic protists are efficiently grazed by crustacean zooplankton. By repackaging their picoplanktonic prey into particles accessible for crustacean grazers, phagotrophic protists represent a crucial link channeling picoplankton production to higher trophic levels (Sherr and Sherr 1988; Gifford 1991). The assimilation of picoplankton by protozoa leads to substantial losses in organic carbon via respiration, which has led to a debate about the quantitative significance of the transfer of picoplankton production to higher trophic levels via protists (Sherr et al. 1987). Especially in systems dominated by metazoan grazers that are able to feed directly on picoplankton (i.e., Daphnia), trophic repackaging may be regarded as a sink of carbon (Stockner and Shortreed 1989). However, zooplankton production is determined not only by the quantity of the available carbon, but also its quality. A considerable amount of research has addressed phytoplankton food quality (Ahlgren et al. 1990), but surprisingly few studies have focused on the nutritional value of protozoa for metazoan grazers. In natural systems, especially in freshwater habitats, the availability of sestonic phosphorus (Elser et al. 2001) can determine zooplankton growth. Ciliates and heterotrophic nanoflagellates (HNFs) are rich in phosphorus (Caron and Goldman 1990; Sanders et al. 1996) and, therefore, might be a high-quality food source for zooplankton. However, elemental content alone is insufficient to predict food quality; and essential lipids such as the (n-3) series of polyunsaturated fatty acids (PUFAs) (Von Elert 2002) and sterols (Von Elert et al. 2003; Martin-Creuzburg and Von Elert 2004) can limit zooplankton growth. Little is known about the lipid composition of heterotrophic protists. The scarce data available suggest that the lipid composition of protozoa depends on the synthetic capacities particular to each species and also on the biochemical composition of their food (Desvilettes et al. 1997; Véra et al. 2001). This might explain the extreme variability in the observed food quality of protozoa for metazoan grazers (Sanders and Wickham 1993). Several studies have reported that heterotrophic protists as the sole food source are of low quality for zooplankton (Sanders et al. 1996; Bec et al. 2003a), whereas others have argued that HNFs feeding on microalgae are a high-quality food for zooplankton (Klein Breteler et al. 1999; Tang et al. 2001; Bec et al. 2003b). These latter studies have also shown that HNFs as an intermediary trophic step enhance the 1 Corresponding author ([email protected]). 2 Present address: Laboratoire de Biologie des Protistes UMR CNRS 6023, Université Blaise Pascal, 63177 Aubière cedex, France. 3 Present address: Department of Animal Ecology I, Universitätsstrasse 30, University of Bayreuth, 95440 Bayreuth, Germany. Acknowledgments This work was supported by a postdoctoral fellowship to A.B. from the Conseil Régional d’Auvergne, France, and by project grant DFG El 179/4-2to E.v.E. from the German Research Foundation.