The succession of epiphytic microalgae conditions fungal community composition: how chytrids respond to blooms of dinoflagellates

Abstract

This study aims to investigate the temporal dynamics of the epiphytic protist community on macroalgae, during the summer months, with a specific focus on fungi, and the interactions between zoosporic chytrid parasites and the proliferation of the dinoflagellates. We employed a combination of environmental sequencing techniques, incubation of natural samples, isolation of target organisms and laboratory experiments. Metabarcoding sequencing revealed changes in the dominant members of the epiphytic fungal community. Initially, fungi comprised < 1% of the protist community, mostly accounted for by Basidiomycota and Ascomycota, but with the emergence of Chytridiomycota during the mature phase of the biofilm, the fungal contribution increased to almost 30%. Chytridiomycota became dominant in parallel with an increase in the relative abundance of dinoflagellates in the community. Microscopy observations showed a general presence of chytrids following the peak proliferation of the dinoflagellate Ostreopsis sp., with the parasite, D. arenysensis as the dominant chytrid. The maximum infection prevalence was 2% indicating host-parasite coexistence. To further understand the in-situ prevalence of chytrids, we characterised the dynamics of the host abundance and prevalence of chytrids through co-culture. These laboratory experiments revealed intraspecific variability of D. arenysensis in its interaction with Ostreopsis, exhibiting a range from stable coexistence to the near-extinction of the host population. Moreover, while chytrids preferentially parasitized dinoflagellate cells, one of the strains examined displayed the ability to utilize pollen as a resource to maintain its viability, thus illustrating a facultative parasitic lifestyle. Our findings not only enrich our understanding of the diversity, ecology, and progression of epiphytic microalgal and fungal communities on Mediterranean coastal macroalgae, but they also shed light on the presence of zoosporic parasites in less-explored benthic habitats.

Newly Identified Diversity of Dinomycetaceae (Rhizophydiales, Chytridiomycota), a Family of Fungal Parasites of Marine Dinoflagellates

“…This widespread coastal distribution of D. gilberthii highlights its adaptability. The role of this species in the dynamics of coastal dinoflagellate blooms could be similar to that studied in D. arenysensis, which varies from host-parasite coexistence (observed in the field and laboratory experiments) to near extinction of the host population (observed in laboratory experiments) (Fernández-Valero et al, 2023).…”

“…The scarcity of these detections can be attributed to inadequate sampling efforts, particularly in regions where these fungi occur prominently, such as in the benthic and epiphytic compartments (Fernández-Valero et al, 2022). Additionally, limitations may arise from the lack of sampling during conditions favorable for chytrid growth, such as microalgal blooms (Fernández-Valero et al, 2023).…”

“…The basal fungal clade of Chytridiomycota includes saprotrophs and parasites that infect diatoms (Duan et al, 2018), dinoflagellates (Fernández-Valero et al, 2022;Lepelletier et al, 2014;Reñé et al, 2022), and other marine microorganisms (Gerphagnon et al, 2013;Xue et al, 2018). Infections lead to the death of host cells and can cause the host population to decline (Van den Wyngaert et al, 2022), but parasite and host populations can also coexist (Fernández-Valero et al, 2023). Fungal-host interactions thus have the potential to shape the structure and diversity of marine microbial communities.…”