Toxins or medicines? Phytoplankton diets mediate host and parasite fitness in a freshwater system

Abstract

Diets must satisfy the everyday metabolic requirements of organisms and can also serve as medicines to combat disease. Currently, the medicinal role of diets is much better understood in terrestrial than in aquatic ecosystems. This is surprising because phytoplankton species synthesize secondary metabolites with known antimicrobial properties. Here, we investigated the medicinal properties of phytoplankton (including toxin-producing cyanobacteria) against parasites of the dominant freshwater herbivore, Daphnia. We fed Daphnia dentifera on green algae and toxic cyanobacteria diets known to vary in their nutritional quality and toxin production, and an additional diet of Microcystis with added pure microcystin-LR. We then exposed Daphnia to fungal and bacterial parasites. Anabaena, Microcystis and Chlorella diets prevented infection of Daphnia by the fungal parasite Metschnikowia, while Nodularia toxins increased offspring production by infected hosts. In contrast to their medicinal effects against Metschnikowia, toxic phytoplankton generally decreased the fitness of Daphnia infected with the bacterial parasite, Pasteuria. We also measured the amount of toxin produced by phytoplankton over time. Concentrations of anatoxin-a produced by Anabaena increased in the presence of Metschnikowia, suggesting parasite-induced toxin production. Our research illustrates that phytoplankton can serve as toxins or medicines for their consumers, depending upon the identity of their parasites.

Keywords: Daphnia; anatoxin; medicines; microcystin; parasite–host interactions; phytoplankton.

Figure 1.

Proportion of Daphnia infected with the fungal parasite Metschnikowia bicuspidata, and the bacterial parasite Pasteuria ramosa, on nine phytoplankton diets. Daphnia were exposed either in single parasite treatments (a) or co-infection treatments (b). Prevalence was calculated as the proportion (means ± s.e.) of infected Daphnia out of all exposed individuals. Note that not all individuals in the co-infection treatments (b) became infected with both parasite species. Abbreviations for phytoplankton names: Ana—Anabaena, Mic—Microcystis, Mic+—Microcystis spiked with additional microcystin, Nod—Nodularia, Ank—Ankistrodesmus, Chla—Chlamydomonas, Chlo—Chlorella, Sce—Scenedesmus, Ulo—Ulothrix. For single Metschnikowia infection n = (10, 9, 9, 10, 10, 10, 8, 10, 9), for single Pasteuria infection n = (10, 9, 8, 9, 9, 7, 9, 10, 10), and for co-infection n = (9, 10, 9, 10, 10, 10, 10, 10, 10) all in order of diet. See electronic supplementary material, table S2 for a summary of the statistical analyses. (Online version in colour.)

Figure 2.

Spore yields from Daphnia infected with (a,b) the fungal parasite Metschnikowia bicuspidata and (c,d) the bacterial parasite Pasteuria ramosa on nine phytoplankton diets. Treatments were either single-parasite infections (a,c) or co-infections with both parasites (b,d). Spore yields are lacking for those treatments in which Daphnia were protected from infection by phytoplankton diet (figure 1). Abbreviations for algal names: Ana—Anabaena, Mic—Microcystis, Mic+—spiked Microcystis, Nod—Nodularia, Ank—Ankistrodesmus, Chla—Chlamydomonas, Chlo—Chlorella, Sce—Scenedesmus, Ulo—Ulothrix. Points are individual replicates and black lines represent means.

Figure 3.

Effect sizes for lifetime offspring production of individual Daphnia infected with (a) fungal and (b) bacterial parasites, and (c) the co-infection treatment. Each point represents Glass's Δ calculated from the mean number of offspring produced by individuals in an infection treatment compared to the mean number of offspring produced by controls. Error bars represent standard error of mean. Note that there are no data for Metschnikowia infections for Daphnia reared on Anabaena, spiked Microcystis or Chlorella diets, because no individuals became infected. Not all individuals exposed to both parasites in the co-infection treatment became co-infected. (Abbreviations for algal names: Ana—Anabaena, Mic—Microcystis, Mic+—spiked Microcystis, Nod—Nodularia, Ank—Ankistrodesmus, Chla—Chlamydomonas, Chlo—Chlorella, Sce—Scenedesmus, Ulo—Ulothrix).

Figure 4.

Medicinal effects of phytoplankton toxins on (a) spore yield of the bacterial parasite Pasteuria, and (b) offspring production by Metschnikowia-infected and uninfected control Daphnia. The algal toxin anatoxin-a (means ± s.e.) appears to be induced (c) by the presence of the fungal pathogen, Metschnikowia, in water. Statistical differences (p < 0.05) in (c) are indicated with an asterisk.