Abstract

The forfeiting of photosynthetic capabilities has occurred independently many times throughout eukaryotic evolution. But almost all non-photosynthetic plants and algae still retain a colorless plastid and an associated genome, which performs fundamental processes apart from photosynthesis. Unfortunately, little is known about the forces leading to photosynthetic loss; this is largely because there is a lack of data from transitional species. Here, we compare the plastid genomes of two “transitional” green algae: the photosynthetic, mixotrophic Auxenochlorella protothecoides and the non-photosynthetic, obligate heterotroph Prototheca wickerhamii. Remarkably, the plastid genome of A. protothecoides is only slightly larger than that of P. wickerhamii, making it among the smallest plastid genomes yet observed from photosynthetic green algae. Even more surprising, both algae have almost identical plastid genomic architectures and gene compositions (with the exception of genes involved in photosynthesis), implying that they are closely related. This close relationship was further supported by phylogenetic and substitution rate analyses, which suggest that the lineages giving rise to A. protothecoides and P. wickerhamii diverged from one another around six million years ago.

Highlights

  • The evolutionary loss of photosynthesis are green algae[11], including the colorless genera Prototheca, Helicosporidium, Polytoma, and Polytomella

  • Further contributing to the plastid DNA (ptDNA) streamlining in A. protothecoides and P. wickerhamii is the lack of plastid inverted repeat elements

  • We showed that the A. protothecoides ptDNA is among the smallest observed from photosynthetic algae, those from the Trebouxiophyceae and Chlorophyceae

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Summary

Introduction

The evolutionary loss of photosynthesis are green algae[11], including the colorless genera Prototheca, Helicosporidium, Polytoma, and Polytomella. The only complete plastid genome sequence available from non-photosynthetic green algae is that of the trebouxiophyte Helicosporidium sp. Partial ptDNA sequence data from Prototheca wickerhamii[14] suggest that its plastid genome is in a “transitional stage” between Helicosporidium and various photosynthetic trebouxiophytes. In the hopes of better understanding the shift from a photoautotrophic to heterotrophic lifestyle, we report and compare the plastid genome sequences of A. protothecoides and P. wickerhamii. Both genomes show a surprising amount of similarities, including severe ptDNA contraction and similar gene orders and gene contents, photosynthesis-related genes notwithstanding. Our results provide interesting clues about the loss of photosynthesis and the evolution of obligate heterotrophy within green algae

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