Inhibition of gut digestive proteases by cyanobacterial diets decreases
infection in a Daphnia host-parasite system
Abstract
1. Secondary metabolites produced by primary producers have a wide range
of functions as well as indirect effects outside the scope of their
direct target. Research suggests that protease inhibitors produced by
cyanobacteria influence grazing by herbivores and may also protect
against parasites of cyanobacteria. In this study we asked whether those
same protease inhibitors produced by cyanobacteria also can influence
interactions of herbivores with their parasites. 2. We used the
Daphnia-Metschnikowia zooplankton host-fungal parasite system to address
this question because it is well documented that cyanobacteria protease
inhibitors suppress trypsin and chymotrypsin in the gut of Daphnia, and
because it is known that Metschnikowia infects via the gut. We tested
the hypothesis that Daphnia gut proteases are necessary for
Metschnikowia spores to be released from their asci. We then also tested
whether diets that decrease trypsin and chymotrypsin activity in the
guts of Daphnia lead to lower levels of infection. 3. Our results show
that chymotrypsin promotes release of the fungal spores from their asci.
Moreover, a diet that strongly inhibited chymotrypsin activity in
Daphnia decreased infection levels, particularly in the most susceptible
Daphnia clones. 4. Our results support the growing literature that
cyanobacterial diets can be beneficial to zooplankton hosts when
challenged by parasites and uncover a mechanism that contributes to the
protective effect of cyanobacterial diets. Specifically, we demonstrate
that host chymotrypsin enzymes promote dehiscence of Metschnikowia
spores; when cyanobacteria inhibit activity of chymotrypsin in hosts,
this most likely traps the spore inside the ascus, preventing the
parasite from puncturing the gut and beginning the infection process. 5.
This study illustrates how secondary metabolites of phytoplankton can
protect herbivores against their own enemies.