Multiple losses of photosynthesis and convergent reductive genome evolution in the colourless green algae Prototheca

Shigekatsu Suzuki,Moriya Ohkuma,Ri-ichiroh Manabe,Rikiya Endoh,Yoshihisa Hirakawa

doi:10.1038/s41598-017-18378-8

Abstract

Autotrophic eukaryotes have evolved by the endosymbiotic uptake of photosynthetic organisms. Interestingly, many algae and plants have secondarily lost the photosynthetic activity despite its great advantages. Prototheca and Helicosporidium are non-photosynthetic green algae possessing colourless plastids. The plastid genomes of Prototheca wickerhamii and Helicosporidium sp. are highly reduced owing to the elimination of genes related to photosynthesis. To gain further insight into the reductive genome evolution during the shift from a photosynthetic to a heterotrophic lifestyle, we sequenced the plastid and nuclear genomes of two Prototheca species, P. cutis JCM 15793 and P. stagnora JCM 9641, and performed comparative genome analyses among trebouxiophytes. Our phylogenetic analyses using plastid- and nucleus-encoded proteins strongly suggest that independent losses of photosynthesis have occurred at least three times in the clade of Prototheca and Helicosporidium. Conserved gene content among these non-photosynthetic lineages suggests that the plastid and nuclear genomes have convergently eliminated a similar set of photosynthesis-related genes. Other than the photosynthetic genes, significant gene loss and gain were not observed in Prototheca compared to its closest photosynthetic relative Auxenochlorella. Although it remains unclear why loss of photosynthesis occurred in Prototheca, the mixotrophic capability of trebouxiophytes likely made it possible to eliminate photosynthesis.

Highlights

Acquisition of photosynthesis occurred in diverse eukaryotes by several endosymbiotic events wherein a photosynthetic organism was engulfed and integrated into a heterotrophic protist[1,2]
The plastid genomes comprised 51.7 kb and 48.2 kb in P. cutis and P. stagnora, respectively (Fig. 1a,b); and these genomes were smaller than that of the plastid genome of P. wickerhamii (55.6 kb) and larger than that of Helicosporidium sp. (37.5 kb) (Table 1). Both plastid genomes were composed of relatively low GC (i.e. 29.7% in P. cutis and 25.7% in P. stagnora)
The P. stagnora plastid genome had 56 genes, including 28 protein-coding genes, 25 tRNAs, and 3 rRNAs. Both species lacked many plastid genes required for photosynthesis

Summary

Introduction

Acquisition of photosynthesis occurred in diverse eukaryotes by several endosymbiotic events wherein a photosynthetic organism was engulfed and integrated into a heterotrophic protist[1,2]. Loss of photosynthesis has occurred in diverse lineages of organisms (e.g. apicomplexans, chlorophytes, cryptophytes, diatoms, dinoflagellates, euglenophytes, and Orobanchaceae species), along with heterotrophic free-living algae, holoparasitic plants, and pathogenic protists[3]. Such non-photosynthetic organisms survive by the uptake of organic carbon from the environment or host cells. Comparative analyses of the plastid and nuclear genomes revealed that the gene content for plastid functions was highly conserved among the non-photosynthetic lineages, and the photosynthesis-related genes have mostly disappeared. Our findings suggest that non-photosynthetic trebouxiophytes have convergently lost a similar set of genes related to photosynthesis

Methods

Results

Conclusion