Evolution of Photorespiratory Glycolate Oxidase among Archaeplastida.

Ramona Kern,Charles Delwiche,Hermann Bauwe,Fabio Facchinelli,Andreas P M Weber,Martin Hagemann

doi:10.3390/plants9010106

Abstract

Photorespiration has been shown to be essential for all oxygenic phototrophs in the present-day oxygen-containing atmosphere. The strong similarity of the photorespiratory cycle in cyanobacteria and plants led to the hypothesis that oxygenic photosynthesis and photorespiration co-evolved in cyanobacteria, and then entered the eukaryotic algal lineages up to land plants via endosymbiosis. However, the evolutionary origin of the photorespiratory enzyme glycolate oxidase (GOX) is controversial, which challenges the common origin hypothesis. Here, we tested this hypothesis using phylogenetic and biochemical approaches with broad taxon sampling. Phylogenetic analysis supported the view that a cyanobacterial GOX-like protein of the 2-hydroxy-acid oxidase family most likely served as an ancestor for GOX in all eukaryotes. Furthermore, our results strongly indicate that GOX was recruited to the photorespiratory metabolism at the origin of Archaeplastida, because we verified that Glaucophyta, Rhodophyta, and Streptophyta all express GOX enzymes with preference for the substrate glycolate. Moreover, an “ancestral” protein synthetically derived from the node separating all prokaryotic from eukaryotic GOX-like proteins also preferred glycolate over l-lactate. These results support the notion that a cyanobacterial ancestral protein laid the foundation for the evolution of photorespiratory GOX enzymes in modern eukaryotic phototrophs.

Highlights

Oxygenic photosynthesis is among the most important biological processes on Earth, because it produces the vast majority of organic carbon and most of the atmospheric oxygen
To evaluate the glycolate oxidase (GOX) phylogeny, we considered a broad spectrum of phyla, including non-photosynthetic species
In the case of underrepresented taxonomic groups, all of the sequences that could be identified as putative GOX proteins were used for the alignment (Table S1)

Summary

Introduction

Oxygenic photosynthesis is among the most important biological processes on Earth, because it produces the vast majority of organic carbon and most of the atmospheric oxygen. This process is thought to have evolved approximately 2.5 billion years ago in cyanobacteria, and was later conveyed into a eukaryotic host cell via endosymbiosis, giving rise to plastids [1,2,3]. 2 of green lineage (Viridiplantae) comprises two major clades, the “classical” green algae (Chlorophyta), and their sister lineage, the charophyte green algae, from which land plants evolved (Streptophyta).

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