Warming increases richness and shapes assemblages of eukaryotic parasitic plankton

Abstract

Background: Anthropogenic activities have led to a global rise in water temperatures, prompting increased interest in how warming affects infectious disease ecology. While most studies have focused on individual host-parasite systems, there is a gap in understanding the impact of warming on multi-host, multi-parasite assemblages in natural ecosystems. To address this gap, we investigated freshwater eukaryotic parasite communities in ten natural lakes near Konin, Poland: five artificially heated and five non-heated "control" lakes. Since 1958, the heated lakes have experienced a mean annual temperature increase of 2 °C due to hot water discharge from two adjacent power plants. We collected seasonal environmental DNA (eDNA) samples from surface waters over a two-year period and applied targeted metabarcoding to compare the richness and distribution of eukaryotic parasites across lake types with a focus on protists and fungi.

Results: Using literature searches and sequence metadata from GenBank, we identified putative parasites which included Alveolates, Stramenopiles, basal Fungi and Ichthyosporeans as well as their associated hosts. Heated lakes harboured distinct parasite assemblages with higher richness of chytrids and aphelids, suggesting thermal preferences among certain freshwater microeukaryotic parasites. Other groups exhibited clear seasonal trends with richness of oomycetes peaking in spring and summer, and that of Cryptomycota in winter and autumn. A general linear model revealed a marginally positive correlation between chytrid parasite richness and richness of their green algal, diatom, and dinoflagellate hosts. Post-hoc analyses indicated that heated lakes exhibited greater seasonal variation in chytrid parasite richness and a stronger correlation between host and parasite richness than control lakes.

Conclusion: These findings demonstrate that warming can induce strong shifts in the richness and assemblages of freshwater microeukaryotic parasites. Using chytrids as a focal group, we additionally demonstrate that warming may amplify seasonal variation in parasite richness and strengthen host-parasite richness relationships.

Fig. 1

Parasite ASV count in the A Protist and B Fungal datasets. Colors represent broad host taxa to which identified hosts of the parasite ASVs belong (see Methods and Fig. S3 for details). Note that Fungal ASVs from the protist dataset were not considered for statistical analyses

Fig. 2

Relative abundances of ASVs indicative of control (left panel) and heated (right panel) lakes. Each square represents the relative abundance of indicator ASVs (rows) in individual lakes (columns), grouped by the season of sampling indicated on the x-axis. Sampling occurred over two consecutive years (See Methods). Of the 39 indicator ASVs identified (Table S5), 29 are presented here as they were present in more than 20% of samples. ASV numbers are specified in brackets. For ASVs in the protist dataset (marked with an asterisk), the lowest taxonomic classification assigned using the PR2 database is reported with values in the blue “%” column indicating sequence similarity to the BLAST hit used to obtain host information (host entry from GenBank metadata). For ASVs from the fungal dataset, the lowest known classification from the BLAST hit is reported, with the blue “%” values indicating sequence similarity between the ASV and the BLAST hit. The classification of E. complanata as a parasite was based on a literature search (Table S5)

Fig. 3

ASV richness of the four most ASV-rich parasite groups: A Chytrids, B Aphelids, C Peronosporomycetes (= Oomycetes) and (D) Cryptomycota. Colors indicate lake type and symbols indicate the season of sample collection. Filled symbols denote individual data points, whereas larger open symbols indicate seasonal mean values. Note that the y-axis scales differ across panels to optimize visualization

Fig. 4

Correlation between chytrid parasite ASV richness (from the fungal dataset) and host ASV richness across Chlorophyta, Charophyta, Chromista, Gyrista, and Dinoflagellata (from the protist dataset). Shaded areas represent 95% confidence intervals. Colors differentiate between lake types, and symbols indicate the season of sample collection