Abstract
Understanding factors that generate, maintain, and constrain host-parasite associations is of major interest to biologists. Although little studied, many extremely virulent micro-eukaryotic parasites infecting microalgae have been reported in the marine plankton. This is the case for Amoebophrya, a diverse and highly widespread group of Syndiniales infecting and potentially controlling dinoflagellate populations. Here, we analyzed the time-scale gene expression of a complete infection cycle of two Amoebophrya strains infecting the same host (the dinoflagellate Scrippsiella acuminata), but diverging by their host range (one infecting a single host, the other infecting more than one species). Over two-thirds of genes showed two-fold differences in expression between at least two sampled stages of the Amoebophrya life cycle. Genes related to carbohydrate metabolism as well as signaling pathways involving proteases and transporters were overexpressed during the free-living stage of the parasitoid. Once inside the host, all genes related to transcription and translation pathways were actively expressed, suggesting the rapid and extensive protein translation needed following host-cell invasion. Finally, genes related to cellular division and components of the flagellum organization were overexpressed during the sporont stage. In order to gain a deeper understanding of the biological basis of the host-parasitoid interaction, we screened proteins involved in host-cell recognition, invasion, and protection against host-defense identified in model apicomplexan parasites. Very few of the genes encoding critical components of the parasitic lifestyle of apicomplexans could be unambiguously identified as highly expressed in Amoebophrya. Genes related to the oxidative stress response were identified as highly expressed in both parasitoid strains. Among them, the correlated expression of superoxide dismutase/ascorbate peroxidase in the specialist parasite was consistent with previous studies on Perkinsus marinus defense. However, this defense process could not be identified in the generalist Amoebophrya strain, suggesting the establishment of different strategies for parasite protection related to host specificity.
Highlights
Parasitism is probably one of the most widespread lifestyles in nature
Cleaned sequence reads from each A120 (342 M) and A25 (160 M) samples were aligned on the gene prediction dataset of the corresponding Amoebophrya strain, yielding high-quality alignments for a significant fraction of the reads (222M for A120 and 122M for A25; Tables S2, S3)
Contrary to the URG1, the URG2 and URG3 groups were defined according to the prevalence and progress of Amoebophrya-infected hosts at each time point of the experiment (Figure S1): while URG2 encompasses genes upregulated at the beginning (T6-T12-T18, corresponding to the passage of the parasite from the cytoplasm to the nucleus of the host cell; Figures S2, S3 panel B and Figures 3B–D), URG3 contains genes upregulated at the end
Summary
Parasitism is probably one of the most widespread lifestyles in nature. The intrinsic relationship established between a parasite and its host implies a delicate and unstable balance, where the parasite subverts the metabolism of the host to fulfill its needs while the host develops strategies allowing it to prevent and survive infection. While most studies are aimed at plant and animal parasites (Torchin and Mitchell, 2004; Hart, 2011; Tellier and Brown, 2011; Kutzer and Armitage, 2016), not much is known about parasites of marine microbes, especially those infecting phytoplanktonic micro-eukaryotes. One example of this overlooked group corresponds to organisms belonging to the Amoebophrya spp. genus (MALV or Marine Alveolates), a diverse clade of parasitoids infecting dinoflagellates, some of them responsible of toxic algal blooms (Cachon, 1964; Park et al, 2004). The high-quality ribosomal RNA database SILVA encompasses today over 2,000 SSU sequences corresponding to Amoebophrya species: only 39 SSU sequences have been described today, labeled as “Amoebophrya sp.,” with more than 2,000 SSU sequences still accounting for uncultured species (Glöckner et al, 2017)
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