Comparison of sterol and fatty acid profiles of chytrids and their hosts reveals trophic upgrading of nutritionally inadequate phytoplankton by fungal parasites

Abstract

Summary Chytrids are ubiquitous fungal parasites in aquatic ecosystems, infecting representatives of all major phytoplankton groups. They repack carbon from inedible phytoplankton hosts into easily ingested chytrid propagules (zoospores), rendering this carbon accessible to zooplankton. Grazing on zoospores may circumvent bottlenecks in carbon transfer imposed by the dominance of inedible or poorly nutritious phytoplankton (mycoloop). We explored qualitative aspects of the mycoloop by analysing lipid profiles (fatty acids, sterols) of two chytrids infecting two major bloom‐forming phytoplankton taxa of contrasting nutritional value: the diatom Asterionella formosa and the filamentous cyanobacterium Planktothrix agardhii. The polyunsaturated fatty acid composition of chytrids largely reflected that of their hosts, highlighting their role as conveyors of otherwise inaccessible essential lipids to higher trophic levels. We also showed that chytrids are capable of synthesizing sterols, thus providing a source of these essential nutrients for grazers even when sterols are absent in their phytoplankton hosts. Our findings reveal novel qualitative facets of the mycoloop, showing that parasitic chytrids, in addition to making carbon and essential lipids available from inedible sources, also upgrade their host's biochemical composition by producing sterols de novo, thereby enhancing carbon and energy fluxes in aquatic food webs.

Essential Biomolecules in Food Webs

“…Eukaryotic fungi are potentially an important resource in aquatic ecosystems, especially in streams (Krauss et al, 2011). The same applies to chytrids, ubiquitous fungal parasites in aquatic ecosystems, providing a sterol source to their grazers even in absence of their phytoplankton hosts (Gerphagnon et al, 2019). Cyanobacteria as prokaryotes do not produce sterols at all (Volkman, 2003).…”

Temperature and host diet jointly influence the outcome of infection in a Daphnia‐fungal parasite system

“…Arguably, rather than a consequence of low food quality per se (i.e. lack of sterols and long-chain poly-unsaturated fatty acids in cyanobacteria; Gerphagnon et al, 2018), our results could also be partially explained by the reported antifungal properties of M. aeruginosa (Sánchez et al, 2019). While the genus Planktothrix has not been tested for its antifungal properties against Daphnia parasites, it produces a wide array of bioactive secondary metabolites (Kurmayer, Deng, & Entfellner, 2016), that are likely to be involved in the defence against fungal chytrid parasites (Rohrlack, Christiansen, & Kurmayer, 2013;Sønstebø & Rohrlack, 2011).…”

Toward Disentangling the Multiple Nutritional Constraints Imposed by Planktothrix: The Significance of Harmful Secondary Metabolites and Sterol Limitation

“…The role of essential lipids in determining the food quality of Planktothrix for zooplankton grazers has not been explored yet. However, sterol production by fungal parasites (chytrids) infecting Planktothrix filaments has been suggested to upgrade the poor food quality of Planktothrix for higher trophic levels (Gerphagnon et al, 2019).…”