Anne Walraven: Revealing the plastid symbioses in the marine centrohelid Meringosphaera: a novel model system for plastid evolution

Abstract

The evolution of photosynthetic organelles, or plastids, through endosymbiosis has been transformative for life on our planet. Yet, many questions remain about the process of endosymbiont integration and organellogenesis. Identifying the different steps leading towards acquisition of a permanent plastid requires studying organisms that are at different stages of plastid integration. In this thesis, we investigate the plastid symbioses in the marine centrohelid Meringosphaera in order to determine their nature and level of genetic and metabolic integration. 

In Paper I, we determine that Meringosphaera has obtained plastids from dictyochophyte algae at least twice independently in two different groups. We suggest that these plastids are kleptoplastids stolen from unknown dictyochophyte prey. We also find evidence of genetic integration of these plastids in the Meringosphaera host genome.

In Paper II, we expand our taxon sampling of Meringosphaera and discover that instead of kleptoplastidy, we find evidence of permanent integration of Meringsophaera’s plastids. We also find more evidence of genetic integration through horizontal gene transfer, including ancestral acquisition of plastid-related genes before Meringosphaera’s plastids were obtained.

In Paper III, we investigate the expanded diversity of both Meringosphaera and dictyochophytes as well as their global biogeography. We find that several Meringosphaera and dictyochophyte amplicon sequence variants (ASVs) co-occur in marine samples, and hypothesize that this co-occurrence may have contributed to Meringosphaera’s preference for dictyochophyte plastid donors.

Finally, in Paper IV, we test a new strategy for targeting and sequencing Meringosphaera single-cells from specific clades, by combining digital PCR (dPCR), cell sorting, and single-cell transcriptomics. We obtain the first four Meringosphaera single-cell transcriptomes and are able to confirm that essential plastid genes as well as host-encoded plastid-targeted genes are transcribed.

In summary, we show that Meringosphaera consists of several clades with different lifestyles, including both plastid-containing and plastid-lacking groups. We also find that Meringosphaera’s plastids are genetically and metabolically integrated into its cell, and that this integration preceded plastid acquisition, supporting current models of plastid evolution. Altogether, we show that Meringosphaera is a diverse and interesting novel model system for studying the evolution of plastids.