Responses of unicellular predators to cope with the phototoxicity of photosynthetic prey

Akihiro Uzuka,Ryo Onuma,Yusuke Kobayashi,Hirofumi Yoshikawa,Takayuki Fujiwara,Shin-Ya Miyagishima,Shunsuke Hirooka,Yu Kanesaki

doi:10.1038/s41467-019-13568-6

Abstract

Feeding on unicellular photosynthetic organisms by unicellular eukaryotes is the base of the aquatic food chain and evolutionarily led to the establishment of photosynthetic endosymbionts/organelles. Photosynthesis generates reactive oxygen species and damages cells; thus, photosynthetic organisms possess several mechanisms to cope with the stress. Here, we demonstrate that photosynthetic prey also exposes unicellular amoebozoan and excavates predators to photosynthetic oxidative stress. Upon illumination, there is a commonality in transcriptomic changes among evolutionarily distant organisms feeding on photosynthetic prey. One of the genes commonly upregulated is a horizontally transferred homolog of algal and plant genes for chlorophyll degradation/detoxification. In addition, the predators reduce their phagocytic uptake while accelerating digestion of photosynthetic prey upon illumination, reducing the number of photosynthetic cells inside the predator cells, as this also occurs in facultative endosymbiotic associations upon certain stresses. Thus, some mechanisms in predators observed here probably have been necessary for evolution of endosymbiotic associations.

Highlights

Feeding on unicellular photosynthetic organisms by unicellular eukaryotes is the base of the aquatic food chain and evolutionarily led to the establishment of photosynthetic endosymbionts/organelles
It appears that the transition from phagotrophy to photoautotrophy occurred through a mixture of the abovementioned mechanisms because mixotrophic predators, which possess photosynthetic plastids of secondary endosymbiotic origin and ingest and digest prey by phagocytosis, are known in several groups of eukaryotes[6,8]
The results of these studies suggest that the absence of phagotrophy in many photosynthetic eukaryotes is due to multiple convergent losses rather than an already established ancestral state of eukaryotes that acquired plastids[11,12]

Summary

Introduction

Feeding on unicellular photosynthetic organisms by unicellular eukaryotes is the base of the aquatic food chain and evolutionarily led to the establishment of photosynthetic endosymbionts/organelles. To examine how the excavate and amoebozoans cope with the phototoxicity of photosynthetic prey, transcriptomic changes in the three species feeding on green prey upon illumination

Results

Conclusion