Temporal Variability and Ecological Interactions of Parasitic Marine Syndiniales in Coastal Protist Communities

Abstract

Syndiniales are a ubiquitous group of protist parasites that infect and kill a wide range of hosts, including harmful bloom-forming dinoflagellates. Despite the importance of parasitism as an agent of plankton mortality, parasite-host dynamics remain poorly understood, especially over time, hindering the inclusion of parasitism in food web and ecosystem models. For a full year in the Skidaway River Estuary (Georgia), we employed weekly 18S rRNA sampling and co-occurrence network analysis to characterize temporal parasite-host infection dynamics of Syndiniales. Over the year, Syndiniales exhibited strong temporal variability, with higher relative abundance from June to October (7 to 28%) than other months in the year (0.01% to 6%). Nonmetric dimensional scaling of Syndiniales composition revealed tight clustering in June to October that coincided with elevated temperatures (23 to 31°C), though in general, abiotic factors poorly explained composition (canonical correspondence analysis [CCA] and partial least-squares [PLS]) and were less important in the network than biotic relationships. Syndiniales amplicon sequence variants (ASVs) were well represented in the co-occurrence network (20% of edges) and had significant positive associations (Spearman r > 0.7), inferred to be putative parasite-host relationships, with known dinoflagellate hosts (e.g., Akashiwo and Gymnodinium) and other protist groups (e.g., ciliates, radiolarians, and diatoms). Positive associations rarely involved a single Syndiniales and dinoflagellate species, implying flexible parasite-host infection dynamics. These findings provide insight into the temporal dynamics of Syndiniales over a full year and reinforce the importance of single-celled parasites in driving plankton population dynamics. Further empirical work is needed to confirm network interactions and to incorporate parasitism within the context of ecosystem models.IMPORTANCE Protist parasites in the marine alveolate group, Syndiniales, have been observed within infected plankton host cells for decades, and recently, global-scale efforts (Tara Ocean exploration) have confirmed their importance within microbial communities. Yet, protist parasites remain enigmatic, particularly with respect to their temporal dynamics and parasite-host interactions. We employed weekly 18S amplicon surveys over a full year in a coastal estuary, revealing strong temporal shifts in Syndiniales parasites, with highest relative abundance during warmer summer to fall months. Though influenced by temperature, Syndiniales population dynamics were also driven by a high frequency of biological interactions with other protist groups, as determined through co-occurrence network analysis. Parasitic interactions implied by the network highlighted a range of confirmed (dinoflagellates) and putative (diatoms) interactions and suggests parasites may be less selective in their preferred hosts. Understanding parasite-host dynamics over space and time will improve our ability to include parasitism as a loss term in microbial food web models.

Keywords: Syndiniales; microbial interactions; network analysis; parasitism; protists.

FIG 1

Relative abundance bar plots of major taxa in the estuary over the year, according to PR2 annotation at the class level (A) and order level (B) within the Syndiniales group. Bar plots are faceted and not stacked to visualize temporal trends for each protist group. Error bars represent the standard deviations from replicate sample means. Taxa included in the “other” category represent <5% of the total protist or Syndiniales community on each respective day. Syndiniales were dominated by three groups (Dino-Groups I, II, and, III), with only a few sequences being unclassified at the order level. Samples from the same month are indicated within brackets on the x axis for all temporal figures (see Table S1 in the supplemental material for exact dates).

FIG 2

Temporal shifts in Shannon alpha diversity and ordination by nonmetric dimensional scaling (NMDS) of the total protist community (A and C) and only Syndiniales (B and D). Alpha diversity values represent mean and standard deviations from replicate samples, while points in the NMDS represent Bray-Curtis distances of communities (based on relative abundance) for each replicate per sample. Sampling days are colored similarly for both diversity metrics according to the observed temperature gradient in the estuary. Stress values for the NMDS are shown.

FIG 3

(A) Filtered co-occurrence network of positive (copresence; blue) and negative (exclusion; orange) edges between Syndiniales ASVs and ASVs from other protist groups. ASVs included in the network were found in >50% of samples. Class-level groups or abiotic factors associated with Syndiniales (labeled nodes) were represented by 2 to 21 ASVs per group. The following classes were represented by <2 ASVs per class and included in the “other” group: Bioecea, Chlorophyceae, Filosa-Thecofilosea, Katablepharidaceae, Nephroselmidophyceae, Pedinophyceae, Porphyridiophyceae, Pyramimonadales, and Trebouxiophyceae. Thicker lines represent more interactions found between Syndiniales and other protist groups. Edges were computed between ASVs based on a suite of correlation and similarity metrics and included if statistically significant (merged q value < 0.05). (B) Total numbers of positive and negative edges connected between Syndiniales and other major groups.

FIG 4

Diagram depicting the presence or absence of Syndiniales-Dinophyceae ASV pairings observed in the filtered network. Colored squares represent either a positive (copresence; blue) or negative (exclusion; orange) association for the respective pairing. Syndiniales parasites are referenced by group (Dino-Group [DG] I, II, or III), while species annotation is shown for dinoflagellates. Dinophyceae ASV 336 represents an unidentified Suessiales taxon. Dark shaded boxes represent edges with merged q values of <0.001, while lighter boxes reflect q values of <0.05.

FIG 5

Relative abundance (%) plots of specific Syndiniales (purple) and Dinophyceae (green) ASV pairings that were found over the year in the estuary. Positive interactions rarely involved a one-to-one interaction (A), more often involving a single Syndiniales or Dinophyceae ASV interacting with >2 ASVs from the other group (B). All ASV-ASV interactions were significant (q values < 0.05) and derived from the filtered network. Error bars represent standard deviations from replicate sample means.