Primary endosymbiosis and the evolution of light and oxygen sensing in photosynthetic eukaryotes.

Nathan C Rockwell,Debashish Bhattacharya,J C Lagarias

doi:10.3389/fevo.2014.00066

Abstract

The origin of the photosynthetic organelle in eukaryotes, the plastid, changed forever the evolutionary trajectory of life on our planet. Plastids are highly specialized compartments derived from a putative single cyanobacterial primary endosymbiosis that occurred in the common ancestor of the supergroup Archaeplastida that comprises the Viridiplantae (green algae and plants), red algae, and glaucophyte algae. These lineages include critical primary producers of freshwater and terrestrial ecosystems, progenitors of which provided plastids through secondary endosymbiosis to other algae such as diatoms and dinoflagellates that are critical to marine ecosystems. Despite its broad importance and the success of algal and plant lineages, the phagotrophic origin of the plastid imposed an interesting challenge on the predatory eukaryotic ancestor of the Archaeplastida. By engulfing an oxygenic photosynthetic cell, the host lineage imposed an oxidative stress upon itself in the presence of light. Adaptations to meet this challenge were thus likely to have occurred early on during the transition from a predatory phagotroph to an obligate phototroph (or mixotroph). Modern algae have recently been shown to employ linear tetrapyrroles (bilins) to respond to oxidative stress under high light. Here we explore the early events in plastid evolution and the possible ancient roles of bilins in responding to light and oxygen.

Highlights

ECOLOGY AND EVOLUTIONPrimary endosymbiosis and the evolution of light and oxygen sensing in photosynthetic eukaryotes
Reviewed by: Denis Baurain, Université de Liège, Belgium James Cotton, Wellcome Trust Sanger Institute, UK Dion G
Plastids are highly specialized compartments derived from a putative single cyanobacterial primary endosymbiosis that occurred in the common ancestor of the supergroup Archaeplastida that comprises the Viridiplantae, red algae, and glaucophyte algae

Summary

ECOLOGY AND EVOLUTION

Primary endosymbiosis and the evolution of light and oxygen sensing in photosynthetic eukaryotes. Three major groups contain what are termed “primary” plastids surrounded by a double membrane: glaucophytes, rhodophytes (red algae), and the Viridiplantae (green algae and land plants) These lineages are putatively united in the monophyletic supergroup Archaeplastida (Adl et al, 2012 [ known as Plantae]), with their common ancestor having captured the plastid via phagotrophic engulfment of a freeliving cyanobacterium (Figure 1). Important for cell evolution and adaptation, these processes confound an unbiased assessment of Archaeplastida monophyly (e.g., Burki et al, 2007; Patron et al, 2007; Parfrey et al, 2010; Grant and Katz, 2014) Alternative approaches such as studying multi-protein complexes or cataloging the origins of individual genes in genome-wide gene inventories are increasingly prevalent in studies of the evolutionary history of primary-plastid-containing algae (e.g., Chan et al, 2011; Price et al, 2012).

Bilins and plastid evolution in algae and plants

CONCLUSION