Sizing up the genomic footprint of endosymbiosis

Abstract

A flurry of recent publications have challenged consensus views on the tempo and mode of plastid (chloroplast) evolution in eukaryotes and, more generally, the impact of endosymbiosis in the evolution of the nuclear genome. Endosymbiont-to-nucleus gene transfer is an essential component of the transition from endosymbiont to organelle, but the sheer diversity of algal-derived genes in photosynthetic organisms such as diatoms, as well as the existence of genes of putative plastid ancestry in the nuclear genomes of plastid-lacking eukaryotes such as ciliates and choanoflagellates, defy simple explanation. Collectively, these papers underscore the power of comparative genomics and, at the same time, reveal how little we know with certainty about the earliest stages of the evolution of photosynthetic eukaryotes.

After the primary endosymbiosis: an update on the chromalveolate hypothesis and the origins of algae with Chl c

“…Out of the 171 red algal genes with very high bootstrap support ([85%) in one or both of the diatom genomes, 11 were shared with oomycetes (Bowler et al 2008), confirming an earlier report (Tyler et al 2006). However, questions have been raised about whether the number of red algal genes is above the background that might be expected due to the occasional acquisition of genes from prey by phagocytic ancestors (Stiller et al 2009;Elias and Archibald 2009). …”

“…This review addresses the complicated evolutionary relationships of the algae with Chl c and their non-photosynthetic relatives. More information can be found in several excellent reviews by Archibald (2009), Elias and Archibald (2009), Keeling (2009Keeling ( , 2010, and Lim and McFadden (2010).…”

Phylogeny and Molecular Evolution of the Green Algae

“…An ancient green algal endosymbiont may also explain the presence of numerous "green" genes in oomycetes (nonphotosynthetic chromalveolates) and apicomplexan parasites (chromalveolates containing nonphotosynthetic plastids of red-algal origin) (Huang et al, 2004;Tyler et al, 2006;Janouškovec et al, 2010). Similarly, the presence of genes related to green algal sequences in trypanosomatid parasites (kinetoplastids) has been explained by EGT of an ancient green algal endosymbiont (Hannaert et al, 2003), but these data are open to interpretation and scenarios of ancient cryptic secondary endosymbioses in the chromalveolates and other eukaryotes have been questioned (Dagan & Martin, 2009b;Elias & Archibald, 2009;Stiller et al, 2009;Sun et al, 2010). In Monosiga, a member of the Choanozoa, which forms the sister group of the Metazoa, numerous genes of putative algal origin are present, including several genes with green algal affinities (Nedelcu et al, 2008;Sun et al, 2010).…”

Plastid Origin and Evolution: New Models Provide Insights into Old Problems

“…These data significantly complicate our understanding of chromalveolate evolution and may be explained by a cryptic green algal endosymbiosis that predated the canonical red algal capture. Under this scenario, the presence of a red alga-derived plastid in many chromalveolates conceals a past endosymbiosis, with the green E/HGTs acting as footprints of this ancient event (for discussion, see Elias and Archibald, 2009;Moustafa et al, 2009). Similarly, whereas the chlorarachniophyte Bigelowiella natans contains a large number of green algaderived nuclear genes to support the function of its green plastid, a significant number of red algalderived, plastid-targeted proteins also exist in this lineage (Archibald et al, 2003).…”