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The thecate amoeba Paulinella is a valuable model for understanding plastid organellogenesis because this lineage has independently gained plastids (termed chromatophores) of alpha-cyanobacterial provenance. Plastid primary endosymbiosis in Paulinella occurred relatively recently (90–140 million years ago, Mya), whereas the origin of the canonical Archaeplastida plastid occurred >1,500 Mya. Therefore, these two events provide independent perspectives on plastid formation on vastly different timescales. Here we generated the complete chromatophore genome sequence from P. longichromatophora (979,356 bp, GC-content = 38.8%, 915 predicted genes) and P. micropora NZ27 (977,190 bp, GC-content = 39.9%, 911 predicted genes) and compared these data to that from existing chromatophore genomes. Our analysis suggests that when a basal split occurred among photosynthetic Paulinella species ca. 60 Mya, only 35% of the ancestral orthologous gene families from the cyanobacterial endosymbiont remained in chromatophore DNA. Following major gene losses during the early stages of endosymbiosis, this process slowed down significantly, resulting in a conserved gene content across extant taxa. Chromatophore genes faced relaxed selection when compared to homologs in free-living alpha-cyanobacteria, likely reflecting the homogeneous intracellular environment of the Paulinella host. Comparison of nucleotide substitution and insertion/deletion events among different P. micropora strains demonstrates that increases in AT-content and genome reduction are ongoing and dynamic processes in chromatophore evolution.

Ciliate Mesodinium species are commonly distributed in diverse aquatic systems worldwide. Among Mesodinium species, M. rubrum is closely associated with microbial food webs and red tide formation and is known to acquire chloroplasts from its cryptophyte prey for use in photosynthesis. For these reasons, Mesodinium has long received much attention in terms of ecophysiology and chloroplast evolution. Mesodinium cells are easily identifiable from other organisms owing to their unique morphology comprising two hemispheres, but a clear distinction among species is difficult under a microscope. Recent taxonomic studies of Mesodinium have been conducted largely in parallel with molecular sequence analysis, and the results have shown that the best-known planktonic M. rubrum in fact comprises eight genetic clades of a M. rubrum/M. major complex. However, unlike the planktonic Mesodinium species, little is known of the genetic diversity of benthic Mesodinium species, and to our knowledge, the present study is the first to explore this. A total of ten genetic clades, including two clades composed of M. chamaeleon and M. coatsi, were found in marine sandy sediments, eight of which were clades newly discovered through this study. We report the updated phylogenetic relationship within the genus Mesodinium comprising heterotrophic/mixotrophic as well as planktonic/benthic species. Furthermore, we unveiled the wide variety of chloroplasts of benthic Mesodinium, which were related to the green cryptophyte Chroomonas/Hemiselmis and the red cryptophyte Rhodomonas/Storeatula/Teleaulax groups.