Multiple parallel origins of parasitic Marine Alveolates.

Microbial eukaryotes are important components of marine ecosystems, and the Marine Alveolates (MALVs) are consistently both abundant and diverse in global environmental sequencing surveys. MALVs are dinoflagellates that are thought to be parasites of other protists and animals, but the lack of data beyond ribosomal RNA gene sequences from all but a few described species means much of their biology and evolution remain unknown. Using single-cell transcriptomes from several MALVs and their free-living relatives, we show that MALVs evolved independently from two distinct, free-living ancestors and that their parasitism evolved in parallel. Phylogenomics shows one subgroup (MALV-II and -IV, or Syndiniales) is related to a novel lineage of free-living, eukaryovorous predators, the eleftherids, while the other (MALV-I, or Ichthyodinida) is related to the free-living predator Oxyrrhis and retains proteins targeted to a non-photosynthetic plastid. Reconstructing the evolution of photosynthesis, plastids, and parasitism in early-diverging dinoflagellates shows a number of parallels with the evolution of their apicomplexan sisters. In both groups, similar forms of parasitism evolved multiple times and photosynthesis was lost many times. By contrast, complete loss of the plastid organelle is infrequent and, when this does happen, leaves no residual genes.

Photosystems in the eye-like organelles of heterotrophic warnowiid dinoflagellates.

Warnowiid dinoflagellates contain a highly complex camera-eye-like structure called the ocelloid that is composed of different organelles resembling parts of metazoan eyes, including a modified plastid that serves as the retinal body.1 The overall structure of the ocelloid has been investigated by microscopy; because warnowiids are not in culture and are rare in nature, we know little about their function.1,2 Here, we generate single-cell transcriptomes from 18 warnowiid cells collected directly from the marine environment representing all 4 known genera and 1 previously undescribed genus, as well as 8 cells from a related lineage, the polykrikoids. Phylogenomic analyses show that photosynthesis was independently lost twice in warnowiids. Interestingly, the non-photosynthetic taxa still express a variety of photosynthesis-related proteins. Nematodinium and Warnowia (known or suspected to be photosynthetic1,3) unsurprisingly express a full complement of photosynthetic pathway components. However, non-photosynthetic genera with ocelloids were also found to express light-harvesting complexes, photosystem I, photosynthetic electron transport (PET), cytochrome b6f, and, in Erythropsidinium, plastid ATPase, representing all major complexes except photosystem II and the Calvin cycle. This suggests that the non-photosynthetic retinal body has retained a reduced but still substantial photosynthetic apparatus that perhaps functions using cyclic electron flow (CEF). This may support ATP synthesis in a reduced capacity, but it is also possible that the photosystem has been co-opted to function as a light-driven proton pump at the heart of the sensory mechanism within the complex architecture of ocelloids.