Fungal parasitism on diatoms alters formation and bio–physical properties of sinking aggregates

Abstract

Phytoplankton forms the base of aquatic food webs and element cycling in diverse aquatic systems. The fate of phytoplankton-derived organic matter, however, often remains unresolved as it is controlled by complex, interlinked remineralization and sedimentation processes. We here investigate a rarely considered control mechanism on sinking organic matter fluxes: fungal parasites infecting phytoplankton. We demonstrate that bacterial colonization is promoted 3.5-fold on fungal-infected phytoplankton cells in comparison to non-infected cells in a cultured model pathosystem (diatom Synedra, fungal microparasite Zygophlyctis, and co-growing bacteria), and even ≥17-fold in field-sampled populations (Planktothrix, Synedra, and Fragilaria). Additional data obtained using the Synedra–Zygophlyctis model system reveals that fungal infections reduce the formation of aggregates. Moreover, carbon respiration is 2-fold higher and settling velocities are 11–48% lower for similar-sized fungal-infected vs. non-infected aggregates. Our data imply that parasites can effectively control the fate of phytoplankton-derived organic matter on a single-cell to single-aggregate scale, potentially enhancing remineralization and reducing sedimentation in freshwater and coastal systems.

Planktonic Marine Fungi: A Review

“…Moreover, chytrid infections may facilitate wider ecosystem functioning upon release of nutrients in surface waters after the lysis of host cells (Kagami et al., 2006). Recent work in lakes using both the Synedra – Zygophlyctis model system and field samples demonstrated that chytrid infections reduced the formation of aggregates, in part by promoting bacterial colonization of parasitized phytoplankton cells (Klawonn, Van den Wyngaert, et al., 2023). Whether such interactions occur in the ocean remains unknown.…”

“…Moreover, it remains uncertain whether marine fungi contribute to the formation and stabilization of particles or they delay and reduce aggregation of particles in the water column. The former has been shown in marine sediments (Damare et al., 2008), while the latter has been demonstrated in freshwater environments (Klawonn et al., 2021; Klawonn, Van den Wyngaert, et al., 2023). The potential for planktonic marine fungi to control organic matter fluxes in the ocean are critically important to consider when examining efficiency and microbial controls of the BCP.…”

Functions of extracellular polymeric substances in partitioning suspended and sinking particles in the upper oceans of two open ocean systems

“…In fact, an experimental study found that viral infection of diatoms led to formation of fast-sinking aggregates involving CSP (Yamada et al 2018). In addition, a recent investigation reported that fungal parasites influenced diatom aggregation processes (Klawonn et al 2023). Future studies are necessary to understand how production and degradation of EPS, driven by bacteria, fungi, and viruses, influence partitioning of suspended and sinking particles by modifying chemical compositions, density, size, porosity, and morphology.…”

Chytrids in Soil Environments: Unique Adaptations and Distributions

“…Batrachochytrium dendrobatidis (order Rhizophydiales) can be considered one of the most important infectious diseases impacting the biodiversity of the amphibian population [26][27][28][29][30]. Members of Chytridiomycota have been associated with phytoplankton, including diatoms, dinoflagellates, and cyanobacteria, as microparasites [31][32][33][34]. They are well documented in bloom events in lakes [35,36] and algal blooms in the Mediterranean Sea [37].…”