Effector Repertoire and Host Transcriptomic Responses in the Tripartite Interaction Between the bloom-forming diatom Coscinodiscus granii, the oomycete Lagenisma coscinodisci and Co-occurring Pedinellale Pteridomonas.

Abstract

Parasitic interactions play a central role in shaping phytoplankton community dynamics. Diatoms are a major phytoplankton group for which many parasites have been describe including chytrids and oomycetes, yet host defense mechanisms remain poorly studied, limiting our understanding of the factors that constrain or promote infection events in natural environments. Major challenges in investigating diatom-parasite interactions include obtaining cultivable host-parasite pairs, maintain stable co-cultures with synchronized infection stages, and harvesting sufficient biomass for molecular analyses such as transcriptomics and metabolomics. To address these challenges, we focused on the bloom-forming diatom Coscinodiscus granii, a large species ({approx}200 {micro}m) to allow manual isolation of single cells. This diatom is naturally infected by Lagenisma coscinodisci, an abundant oomycete occasionally observed in temperate coastal environments. We assembled high-quality transcriptomes for both C. granii and L. coscinodisci, providing an important resource for future molecular studies. Transcriptome analyses revealed a sophisticated effector repertoire in L. coscinodisci, including canonical oomycete virulence factors such as Crinklers, RxLR effectors, cystatins, transposon-associated proteins, and components of the RNA interference machinery (Argonaute, Dicer, RdRP), as well as cyclophilins. In the differential gene expression analyses, C. granii exhibited a transcriptional response involving proteases and exosome-related pathways, suggesting a deeply conserved, defense mechanism. In parallel, we analysed the differential expression of the heterotrophic flagellate Pteridomonas sp., which consistently co-occurred in culture, and identified a distinct transcriptional profile characterized by the upregulation of motility-related genes, highlighting a striking mobility strategy. Owing to the exceptionally large host size and the availability of both transcriptomic and metabolomic data, this tripartite system provides a unique marine model for exploring oomycete-diatom interactions.