The tiny enslaved genome of a rhizarian alga

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Abstract
At least twice in the history of life a predatory nonphotosynthetic protozoan cell ate a eukaryotic algal cell and enslaved it internally instead of digesting it, thereby becoming a chimeric photophagotrophic cell with two distinct nuclei and remarkably complex membrane topology—far surpassing that of animals or plants. In their descendants, the host nucleus became dominant, whereas that of the algal slave shrank by transfer of most of its genes into the main nucleus and retargeting the proteins they encode back into the enslaved chloroplast. Some descendants managed to transfer all essential genes and lose the enslaved nuclei altogether while retaining the algal chloroplast and plasma membrane (e.g., brown seaweeds), but in two groups of algae, cryptomonads (1) and chlorarachneans (2–4), the enslaved nucleus remains in the chimeric cell many millions of years afterward, raising fascinating questions for cell and evolutionary biology. How are functions shared between two evolutionarily unrelated nuclei, and how do their proteins integrate into one harmonious cell? The first inklings of answers came with the first nucleomorph genome sequence from a cryptomonad (1). In this issue of PNAS, Gilson et al. (5) report the first genome sequence of a chlorarachnean nucleomorph, the tiniest nucleus in nature. Fig. 1 shows how these two unusual algal groups fit on the eukaryote evolutionary tree (6, 7). Cryptomonads belong to a vast branch, the chromalveolates, formed by a single enslavement of a red alga (8, 9) and containing eight phyla: two mainly photosynthetic [Ochrophyta (including brown algae, diatoms, and eight other algal classes) and Haptophyta]; two with one algal class each (dinoflagellates and cryptomonads) but many heterotrophs; and four entirely nonphotosynthetic (e.g., ciliate protozoa, and Pseudofungi) (10). By contrast, chlorarachneans belong to Rhizaria, a typically amoeboid group characterized by long, thin-branching pseudopods that often anastomose as a … *E-mail: tom.cavalier-smith{at}zoo.ox.ac.uk