Independent evolution of the thioredoxin system in photosynthetic Paulinella species

Abstract

Redox regulation allows phytoplankton to monitor and stabilize metabolic pathways under changing conditions1. In plastids, the thioredoxin (TRX) system is linked to photosynthetic electron transport and fine tuning of metabolic pathways to fluctuating light levels. Expansion of the number of redox signal transmitters and their protein targets, as seen in plants, is believed to increase cell robustness2. In this study, we searched for genes related to redox regulation in the photosynthetic amoeba Paulinella micropora KR01 (hereafter, KR01). The genus Paulinella includes testate filose amoebae, in which a single clade acquired a photosynthetic organelle, the chromatophore, from an alpha-cyanobacterial donor3. This independent primary endosymbiosis occurred relatively recently (∼124 million years ago) when compared to Archaeplastida (>1 billion years ago), making photosynthetic Paulinella a valuable model for studying the early stages of primary endosymbiosis4. Our comparative analysis demonstrates that this lineage has evolved a TRX system similar to other algae, relying, however, on genes with diverse phylogenetic origins (including the endosymbiont, host, bacteria, and red algae). One TRX of eukaryotic provenance is targeted to the chromatophore, implicating host–endosymbiont coordination of redox regulation. A chromatophore-targeted glucose-6-phosphate dehydrogenase (G6PDH) of red algal origin suggests that Paulinella exploited the existing redox regulation system in Archaeplastida to foster integration. Our study elucidates the independent evolution of the TRX system in photosynthetic Paulinella, whose parts derive from the existing genetic toolkit in diverse organisms.