Abstract
The evolution of an obligate parasitic lifestyle is often associated with genomic reduction, in particular with the loss of functions associated with increasing host-dependence. This is evident in many parasites, but perhaps the most extreme transitions are from free-living autotrophic algae to obligate parasites. The best-known examples of this are the apicomplexans such as Plasmodium, which evolved from algae with red secondary plastids. However, an analogous transition also took place independently in the Helicosporidia, where an obligate parasite of animals with an intracellular infection mechanism evolved from algae with green primary plastids. We characterised the nuclear genome of Helicosporidium to compare its transition to parasitism with that of apicomplexans. The Helicosporidium genome is small and compact, even by comparison with the relatively small genomes of the closely related green algae Chlorella and Coccomyxa, but at the functional level we find almost no evidence for reduction. Nearly all ancestral metabolic functions are retained, with the single major exception of photosynthesis, and even here reduction is not complete. The great majority of genes for light-harvesting complexes, photosystems, and pigment biosynthesis have been lost, but those for other photosynthesis-related functions, such as Calvin cycle, are retained. Rather than loss of whole function categories, the predominant reductive force in the Helicosporidium genome is a contraction of gene family complexity, but even here most losses affect families associated with genome maintenance and expression, not functions associated with host-dependence. Other gene families appear to have expanded in response to parasitism, in particular chitinases, including those predicted to digest the chitinous barriers of the insect host or remodel the cell wall of Helicosporidium. Overall, the Helicosporidium genome presents a fascinating picture of the early stages of a transition from free-living autotroph to parasitic heterotroph where host-independence has been unexpectedly preserved.
Highlights
Helicosporidia are parasitic protists characterized by mature discoid cysts each containing a single filamentous and three ovoid cells [1,2]
Its evolutionary origins were unclear for almost a century, but molecular analysis and surprisingly showed that it is a green alga, which means it has undergone an evolutionary transition from autotrophy to parasitism comparable to that of the malaria parasite Plasmodium and its relatives
Fossils records and molecular clock analyses suggest that Trebouxiophytes as a group arose in the early Neoproterozoic [13], from which the trebouxiophycean subgroup Chorellales later emerged around 100 million years ago [14]. Both Helicosporidium and the non-photosynthetic trebouxiophycean Prototheca arose from within the Chorellales [13], so the adaption to parasitism in Helicosporidia occurred less than 100 mya
Summary
Helicosporidia are parasitic protists characterized by mature discoid cysts each containing a single filamentous and three ovoid cells [1,2]. These parasites invade their invertebrate hosts per os and initiate their replicative stage within the digestive tract [3,4]. The ovoid cells remain in the gut lumen whereas the uncoiled and barbed filamentous cells penetrate the peritrophic membrane and become anchored to the host midgut cells. In the hemocoel the filament cells will transition to a vegetative stage that replicates by autosporulation; a select number at the four-cell stage will differentiate to the infectious cyst stage characterized by the three ovoid and a single filament cell [5,6]. Unlike many parasites the vegetative cells of Helicosporidia can be cultured readily on defined media with limited nutrients, suggesting that despite being a parasitic species, they have retained a diverse slate of metabolic pathways allowing for saprobic growth
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