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Evolution of free-living relatives of apicomplexan parasites Janouškovec, Jan

Abstract

As obligate parasites of animals and humans, apicomplexan parasites contain many unique characteristics that are critical to their lifestyle, but bear little resemblance to other eukaryotes. Several free-living relatives of apicomplexans represent a great potential in understanding early apicomplexan evolution. The photosynthetic Chromera velia provides a particular promise in addressing the long-contentious origin of the apicomplexan plastid. The data presented here provides evidence that the photosynthetic plastids in Chromera velia and another novel alga, CCMP3155 (later named Vitrella brassicaformis), are closely and specifically related to the apicomplexan plastid, and that they together are related to plastids in dinoflagellates. The ancestral plastid went through an unusual reduction in gene content and acquired unique features such as Rubisco II and transcript oligouridylylation. The plastid genome in C. velia is interesting on its own. Two proteins of Photosystem I and ATP synthase have been split to two fragments, which are independently expressed. The genome also appears to exist prevailingly as a linear monomer. These, and additional unprecedented features, redefine our understanding of plastid genome architecture and point to intra-chromosomal recombination as a putative driving force. Assessing environmental distribution of the newly-discovered Chromera and Vitrella leads to a discovery of six additional apicomplexan-related linages (ARLs) comprising 1,316 sequences primarily from coral reefs environments. The most abundant lineage, ARL-V, is novel and exclusively associated with coral tissue and surface samples. ARL-V is present in at least 20 species of symbiotic corals across time and space, which suggests that its relationship with corals is of potential significance to the reef ecosystem. Successful culturing of five Colponema isolates provides the first molecular data for another apicomplexan relative. The genus represents two independent lineages, one of which is the closest sister to apicomplexans and dinoflagellates. Mitochondrial genome data from both lineages reveals a gene-rich content and suggests that a linear monomeric structure with telomeres was ancestral to all alveolates. Altogether, this data illustrates the significance of Chromera, Vitrella, Colponema and several uncultured lineages in illuminating early evolution in apicomplexans and alveolates.

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Attribution-NonCommercial-NoDerivatives 4.0 International