A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids

Abstract

The discovery of a nonphotosynthetic plastid in malaria and other apicomplexan parasites has sparked a contentious debate about its evolutionary origin. Molecular data have led to conflicting conclusions supporting either its green algal origin or red algal origin, perhaps in common with the plastid of related dinoflagellates. This distinction is critical to our understanding of apicomplexan evolution and the evolutionary history of endosymbiosis and photosynthesis; however, the two plastids are nearly impossible to compare due to their nonoverlapping information content. Here we describe the complete plastid genome sequences and plastid-associated data from two independent photosynthetic lineages represented by Chromera velia and an undescribed alga CCMP3155 that we show are closely related to apicomplexans. These plastids contain a suite of features retained in either apicomplexan (four plastid membranes, the ribosomal superoperon, conserved gene order) or dinoflagellate plastids (form II Rubisco acquired by horizontal transfer, transcript polyuridylylation, thylakoids stacked in triplets) and encode a full collective complement of their reduced gene sets. Together with whole plastid genome phylogenies, these characteristics provide multiple lines of evidence that the extant plastids of apicomplexans and dinoflagellates were inherited by linear descent from a common red algal endosymbiont. Our phylogenetic analyses also support their close relationship to plastids of heterokont algae, indicating they all derive from the same endosymbiosis. Altogether, these findings support a relatively simple path of linear descent for the evolution of photosynthesis in a large proportion of algae and emphasize plastid loss in several lineages (e.g., ciliates, Cryptosporidium, and Phytophthora).Apicomplexa | Chromera velia | CCMP3155 | plastid evolution | chloroplast genome

Wider than Thought Phylogenetic Occurrence of Apicortin, A Characteristic Protein of Apicomplexan Parasites

“…These photosynthetic algae are closely related to apicomplexan parasites and share various morphological and molecular characteristics with them. Former phylogenetic analysis strongly and consistently supported it; they either form two distinct lineages with V. brassicaformis more closely related to apicomplexans (Janouškovec et al 2010) or are sisters to them (Woo et al 2015). According to the present analysis, one of the apicortin paralogs in both species, Vbra_15441 from V. brassicaformis and Cvel_6797 from C. velia, is sister to apicomplexan orthologs.…”

How life changes itself: The Read–Write (RW) genome

“…Secondary and tertiary endosymbiosis involving both red and green algae are further responsible for the evolution of a number of additional photosynthetic eukaryotic lineages [107][108][109]. Secondary endosymbiogenetic organisms contain at least four separate genomic compartments: nucleus, mitochondrion, plastid and nucleomorph (the former nucleus of the endosymbiotic alga).…”

Oxygenic photosynthesis and the distribution of chloroplasts

“…In spite of numerous publications, the debate continues (cf. in Green 2010;Baurian et al 2010;Deschamps and Moreira 2009;Janouškovec et al 2010;Keeling 2010;Nozaki et al 2009;Ryes-Prieto et al 2008;Stiller 2007 was one chloroplast origin, and if so, what was the most likely host, i.e., is there only one Cinderella slipper and where is the best fit? Some unambiguous structural signs of symbiotic and/or endosymbiotic events were found some years ago when Gibbs (1981) provided significant examples showing that some chloroplasts had two limiting membranes (green and red algae), others were surrounded by three membranes (euglenids, dinoflagellates), while still others had four chloroplast membranes (browns, diatoms, cryptophytes) usually with an additional set of ribosomes on the ''chloroplast endoplasmic reticulum.''…”

“…Nevertheless, the group has been at the center of the chloroplast dispersion controversy mostly because it has been placed as endosymbiont at the base of the chromalveolates, argued to be a monophyletic evolutionary group (Cavalier-Smith 2002;cf. Green 2010;Janouškovec et al 2010). The chromalveolates are a diverse grouping distinguished by: the presence of Chl a plus Chl c, carotenoid-type fucoxanthin or peridinin, having ciliated or flagellated hosts, and by some un-pigmented members having presumably lost a once functioning integrated chloroplast.…”