Chromera velia, Endosymbioses and the Rhodoplex Hypothesis—Plastid Evolution in Cryptophytes, Alveolates, Stramenopiles, and Haptophytes (CASH Lineages)

Abstract

The discovery of Chromera velia, a free-living photosynthetic relative of apicomplexan pathogens, has provided an unexpected opportunity to study the algal ancestry of malaria parasites. In this work, we compared the molecular footprints of a eukaryote-to-eukaryote endosymbiosis in C. velia to their equivalents in peridinin-containing dinoflagellates (PCD) to reevaluate recent claims in favor of a common ancestry of their plastids. To this end, we established the draft genome and a set of full-length cDNA sequences from C. velia via next-generation sequencing. We documented the presence of a single coxI gene in the mitochondrial genome, which thus represents the genetically most reduced aerobic organelle identified so far, but focused our analyses on five “lucky genes” of the Calvin cycle. These were selected because of their known support for a common origin of complex plastids from cryptophytes, alveolates (represented by PCDs), stramenopiles, and haptophytes (CASH) via a single secondary endosymbiosis with a red alga. As expected, our broadly sampled phylogenies of the nuclear-encoded Calvin cycle markers support a rhodophycean origin for the complex plastid of Chromera. However, they also suggest an independent origin of apicomplexan and dinophycean (PCD) plastids via two eukaryote-to-eukaryote endosymbioses. Although at odds with the current view of a common photosynthetic ancestry for alveolates, this conclusion is nonetheless in line with the deviant plastome architecture in dinoflagellates and the morphological paradox of four versus three plastid membranes in the respective lineages. Further support for independent endosymbioses is provided by analysis of five additional markers, four of them involved in the plastid protein import machinery. Finally, we introduce the “rhodoplex hypothesis” as a convenient way to designate evolutionary scenarios where CASH plastids are ultimately the product of a single secondary endosymbiosis with a red alga but were subsequently horizontally spread via higher-order eukaryote-to-eukaryote endosymbioses.

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

“…At one extreme are the giant mtDNAs of seed plants, like cucumber (∼1.6 Mb) (49) and Silene conica (∼11 Mb) (40), as well as those of diplonemids, which can exceed 500 kb (51). At the other end of the spectrum are the 6-kb mtDNAs of certain apicomplexans (56) and the fragmented mtDNA of their close relative C. velia, which is even smaller (57). Diminutive mtDNAs (<13 kb) have also been uncovered in green algae (44), ctenophores (58), and fungi (59).…”

“…As with size and structure, mtDNAs show greater variation in gene number and organization than ptDNAs (12). The jakobid Andalucia godoyi has the largest, least-derived mitochondrial gene content (100 genes, ∼66 of which encode proteins) (67), whereas dinoflagellates, apicomplexans, and their close relatives have the most reduced: three or fewer proteins, no tRNAs, and in some instances (e.g., C. velia) even lack complete rRNAs (36,56,57,68). Chlamydomonadalean mtDNAs also have diminished coding contents (10-13 genes) (44), and some land plants (e.g., S. moellendorffii), animals (e.g., the winged box jellyfish), and trypanosomes have lost all or most of their mitochondrial tRNA-coding regions (39,42,48).…”

The Roles of Mutation, Selection, and Expression in Determining Relative Rates of Evolution in Mitochondrial versus Nuclear Genomes

“…For example, the large mt genome of the jakobid Andalucia godoyi contains 100 genes (Burger et al 2013). In contrast, the tiny mt genome of the alveolate Chromera velicia appears to contain only a single gene (Petersen et al 2014), and some parasitic and anaerobic eukaryotes have entirely lost their electron transport chain and mt genome (Hjort et al 2010;Karnkowska et al 2016). The variation in the number of mt genes across eukaryotes largely stems from the process of endosymbiotic gene loss and transfer to the nuclear genome that is ongoing in many lineages (Adams and Palmer 2003;Timmis et al 2004).…”

Genomic perspectives on the birth and spread of plastids

“…Or it could mean that it is simpler. It will be interesting to see how the outlier data of Stiller et al (74) stack up against traditional gene-by-gene phylogenomic results, including the "rhodoplex hypothesis" of Petersen et al (112). These are hypotheses that can be tested by seeing whether there are indeed significant patterns of gene exchange between candidate plastid donors and recipients.…”