Abstract
BackgroundThe evolution of photosynthesis has been a major driver in eukaryotic diversification. Eukaryotes have acquired plastids (chloroplasts) either directly via the engulfment and integration of a photosynthetic cyanobacterium (primary endosymbiosis) or indirectly by engulfing a photosynthetic eukaryote (secondary or tertiary endosymbiosis). The timing and frequency of secondary endosymbiosis during eukaryotic evolution is currently unclear but may be resolved in part by studying cryptomonads, a group of single-celled eukaryotes comprised of both photosynthetic and non-photosynthetic species. While cryptomonads such as Guillardia theta harbor a red algal-derived plastid of secondary endosymbiotic origin, members of the sister group Goniomonadea lack plastids. Here, we present the genome of Goniomonas avonlea—the first for any goniomonad—to address whether Goniomonadea are ancestrally non-photosynthetic or whether they lost a plastid secondarily.ResultsWe sequenced the nuclear and mitochondrial genomes of Goniomonas avonlea and carried out a comparative analysis of Go. avonlea, Gu. theta, and other cryptomonads. The Go. avonlea genome assembly is ~ 92 Mbp in size, with 33,470 predicted protein-coding genes. Interestingly, some metabolic pathways (e.g., fatty acid biosynthesis) predicted to occur in the plastid and periplastidal compartment of Gu. theta appear to operate in the cytoplasm of Go. avonlea, suggesting that metabolic redundancies were generated during the course of secondary plastid integration. Other cytosolic pathways found in Go. avonlea are not found in Gu. theta, suggesting secondary loss in Gu. theta and other plastid-bearing cryptomonads. Phylogenetic analyses revealed no evidence for algal endosymbiont-derived genes in the Go. avonlea genome. Phylogenomic analyses point to a specific relationship between Cryptista (to which cryptomonads belong) and Archaeplastida.ConclusionWe found no convincing genomic or phylogenomic evidence that Go. avonlea evolved from a secondary red algal plastid-bearing ancestor, consistent with goniomonads being ancestrally non-photosynthetic eukaryotes. The Go. avonlea genome sheds light on the physiology of heterotrophic cryptomonads and serves as an important reference point for studying the metabolic “rewiring” that took place during secondary plastid integration in the ancestor of modern-day Cryptophyceae.
Highlights
The evolution of photosynthesis has been a major driver in eukaryotic diversification
Eukaryotic operational taxonomic units (OTUs) are colored according to their known or predicted “supergroup” affinities with sequences from Go. avonlea and predicted Gu. theta endosymbiotic gene transfer (EGT) [17] highlighted in bright red (Viridiplantae are in green, Glaucophyta are in turquoise, Rhodophyta are in dark red, Cyanobacteria are orange and other Bacteria are in gold, Cryptophyta are in pink, Haptophyta are in purple, Stramenopiles are in dark blue, Alveolata are in blue, Rhizaria are in light blue)
Sequences are colored according to their taxonomic affiliation: Viridiplantae are in green, Glaucophyta are in turquoise, Rhodophyta are in dark red, Cyanobacteria are orange and other Bacteria are in gold, Cryptophyta are in pink, Goniomonas avonlea is dark red and bolded, Haptophyta are in purple, Stramenopiles are in dark blue, Alveolata are in blue, Rhizaria are in light blue
Summary
The evolution of photosynthesis has been a major driver in eukaryotic diversification. The timing and frequency of secondary endosymbiosis during eukaryotic evolution is currently unclear but may be resolved in part by studying cryptomonads, a group of single-celled eukaryotes comprised of both photosynthetic and non-photosynthetic species. While cryptomonads such as Guillardia theta harbor a red algal-derived plastid of secondary endosymbiotic origin, members of the sister group Goniomonadea lack plastids. Secondary (and in some cases tertiary) endosymbiosis is thought to have given rise to plastids scattered amongst the stramenopiles, alveolates, rhizarians, euglenozoans, haptophytes, and cryptomonads [6] The latter lineage is divided into two clades, the plastid-bearing, mostly photosynthetic Cryptophyceae and the heterotrophic Goniomonadea. The evolutionary distinctness of these two clades makes for an interesting case study with which to understand the transition from a plastid-lacking eukaryote to a photosynthetic, secondary plastid-bearing organism
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