Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome

Abstract

Plastids are supported by a wide range of proteins encoded within the nucleus and imported from the cytoplasm. These plastid-targeted proteins may originate from the endosymbiont, the host, or other sources entirely. Here, we identify and characterise 770 plastid-targeted proteins that are conserved across the ochrophytes, a major group of algae including diatoms, pelagophytes and kelps, that possess plastids derived from red algae. We show that the ancestral ochrophyte plastid proteome was an evolutionary chimera, with 25% of its phylogenetically tractable nucleus-encoded proteins deriving from green algae. We additionally show that functional mixing of host and plastid proteomes, such as through dual-targeting, is an ancestral feature of plastid evolution. Finally, we detect a clear phylogenetic signal from one ochrophyte subgroup, the lineage containing pelagophytes and dictyochophytes, in plastid-targeted proteins from another major algal lineage, the haptophytes. This may represent a possible serial endosymbiosis event deep in eukaryotic evolutionary history.DOI: http://dx.doi.org/10.7554/eLife.23717.001

Horizontal and endosymbiotic gene transfer in early plastid evolution

“…Similarly, recent estimates have suggested that c . 25% of nucleus‐encoded plastid‐targeted proteins in the ancestor of ochrophytes (photosynthetic stramenopiles) have derived from green algae (Dorrell et al ., ). This apparent massive genetic mosaicism may be explained either as the result of a high frequency of eukaryote‐to‐eukaryote HGT or as the consequence of putative cryptic endosymbioses.…”

“…For instance, despite diatoms containing plastids clearly derived from red algae, phylogenetic analysis of diatom nuclear genomes has suggested that > 1700 nucleus-encoded genes were apparently transferred from green algae (Moustafa et al, 2009). Similarly, recent estimates have suggested that c. 25% of nucleus-encoded plastid-targeted proteins in the ancestor of ochrophytes (photosynthetic stramenopiles) have derived from green algae (Dorrell et al, 2017). This apparent massive genetic mosaicism may be explained either as the result of a high frequency of eukaryote-to-eukaryote HGT or as the consequence of putative cryptic endosymbioses.…”

Dictyochophyceae Plastid Genomes Reveal Unusual Variability in Their Organization

“…, Dorrell et al. , Leonard et al. ), the monophyly of the ochrophyte members of the stramenopiles strongly suggests that these groups radiated from a plastid‐bearing and photosynthetic ancestor, with any non‐photosynthetic members within them originating through secondary losses of photosynthesis (Ševčíková et al.…”

“…The distinctive feature of the photosynthetic stramenopiles, in relation to other stramenopiles, is their possession of plastids acquired through secondary or higher endosymbiosis with a red alga or one of its subsequent evolutionary derivatives. Despite the existence of numerous non-photosynthetic organisms within stramenopiles (Patterson 1989, Sekiguchi et al 2002, Cavalier-Smith and Chao 2006, including basally divergent lineages with limited evidence for a photosynthetic ancestry (Stiller et al 2014, Dorrell et al 2017, Leonard et al 2018, the monophyly of the ochrophyte members of the stramenopiles strongly suggests that these groups radiated from a plastid-bearing and photosynthetic ancestor, with any non-photosynthetic members within them originating through secondary losses of photosynthesis ( Sev c ıkov a et al 2015, Derelle et al 2016).…”

Unlocking the biological potential ofEuglena gracilis: evolution, cell biology and significance to parasitism

“…While it was initially thought that organisms possessing plastids of red versus green algal origins would have exclusively or overwhelmingly genes derived from transfer of endosymbiont genes to their nuclei, this is increasingly recognized as simplistic (Curtis et al, 2012, Dorrell et al, 2017. Since plastid acquisition in euglenoids is a relatively recent event, we sought to investigate the evolutionary origins of the genes derived from gene transfer.…”