Chytrids enhance Daphnia fitness by selectively retained chytrid-synthesised stearidonic acid and conversion of short-chain to long-chain polyunsaturated fatty acids

Chytrid fungal parasites convert dietary energy and essential dietary molecules, such as long-chain (LC) polyunsaturated fatty acids (PUFA), from inedible algal/cyanobacteria hosts into edible zoospores. How the improved biochemical PUFA composition of chytrid-infected diet may extend to zooplankton, linking diet quality to consumer fitness, remains unexplored. Here, we assessed the trophic role of chytrids in supporting dietary energy and PUFA requirements of the crustacean zooplankton Daphnia, when feeding on the filamentous cyanobacterium Planktothrix. Only Daphnia feeding on chytrid-infected Planktothrix reproduced successfully and had significantly higher survival and growth rates compared with Daphnia feeding on the sole Planktothrix diet. While the presence of chytrids resulted in a two-fold increase of carbon ingested by Daphnia, carbon assimilation increased by a factor of four, clearly indicating enhanced carbon transfer efficiency with chytrid presence. Bulk carbon (delta C-13) and nitrogen (delta N-15) stable isotopes did not indicate any treatment-specific dietary effects on Daphnia, nor differences in trophic position among diet sources and the consumer. Compound-specific carbon isotopes of fatty acids (delta C-13(FA)), however, revealed that chytrids bioconverted short-chain to LC-PUFA, making it available for Daphnia. Chytrids synthesised the omega-3 PUFA stearidonic acid de novo, which was selectively retained by Daphnia. Values of delta C-13(FA) demonstrated that Daphnia also bioconverted short-chain to LC-PUFA. We provide isotopic evidence that chytrids improved the dietary provision of LC-PUFA for Daphnia and enhanced their fitness. We argue for the existence of a positive feedback loop between enhanced Daphnia growth and herbivory in response to chytrid-mediated improved diet quality. Chytrids upgrade carbon from the primary producer and facilitate energy and PUFA transfer to primary consumers, potentially also benefitting upper trophic levels of pelagic food webs.