Horizontal and endosymbiotic gene transfer in early plastid evolution

Abstract

Plastids evolved from a cyanobacterium that was engulfed by a heterotrophic eukaryotic host and became a stable organelle. Some of the resulting eukaryotic algae entered into a number of secondary endosymbioses with diverse eukaryotic hosts. These events had major consequences on the evolution and diversification of life on Earth. Although almost all plastid diversity derives from a single endosymbiotic event, the analysis of nuclear genomes of plastid-bearing lineages has revealed a mosaic origin of plastid-related genes. In addition to cyanobacterial genes, plastids recruited for their functioning eukaryotic proteins encoded by the host nucleus and also bacterial proteins of noncyanobacterial origin. Therefore, plastid proteins and plastid-localised metabolic pathways evolved by tinkering and using gene toolkits from different sources. This mixed heritage seems especially complex in secondary algae containing green plastids, the acquisition of which appears to have been facilitated by many previous acquisitions of red algal genes (the 'red carpet hypothesis').

Keywords: Paulinella; Archaeplastida; Cyanobacteria; endosymbiosis; evolution; gene transfer; plastids.

Fig. 1

The distribution of photosynthesis in the eukaryotic global phylogeny. Colored solid branches correspond to photosynthetic lineages endowed with primary plastids and colored dashed branches to lineages with secondary plastids (green and red colors indicate the type of secondary endosymbiont, green or red algae, respectively). Blue arrows show the two known primary endosymbioses (in Archaeplastida and Paulinella) and green and red arrows indicate the secondary endosymbioses involving green and red algal endosymbionts. Grey branches correspond to non-photosynthetic eukaryotic phyla. The tree has been largely modified from Adl et al., 2012.

Fig. 2

Light microscopy image of Paulinella chromatophora. The pigmented Synechococcus-like primary plastids are easily visible within the cytoplasm. Scale bar: 10 µm. Image courtesy of Eva Nowack (Heinrich-Heine-Universität Düsseldorf).