Abstract

Genome analysis of the pico-eukaryotic marine green alga Prasinoderma coloniale CCMP 1413 unveils the existence of a novel phylum within green plants (Viridiplantae), the Prasinodermophyta, which diverged before the split of Chlorophyta and Streptophyta. Structural features of the genome and gene family comparisons revealed an intermediate position of the P. coloniale genome (25.3 Mb) between the extremely compact, small genomes of picoplanktonic Mamiellophyceae (Chlorophyta) and the larger, more complex genomes of early-diverging streptophyte algae. Reconstruction of the minimal core genome of Viridiplantae allowed identification of an ancestral toolkit of transcription factors and flagellar proteins. Adaptations of P. coloniale to its deep-water, oligotrophic environment involved expansion of light-harvesting proteins, reduction of early light-induced proteins, evolution of a distinct type of C4 photosynthesis and carbon-concentrating mechanism, synthesis of the metal-complexing metabolite picolinic acid, and vitamin B1, B7 and B12 auxotrophy. The P. coloniale genome provides first insights into the dawn of green plant evolution.

Highlights

  • One of the most important biological events in the history of life was the successful colonization of the terrestrial landscape by green plants (Viridiplantae) that paved the way for terrestrial animal evolution, altering geomorphology and changes in the Earth’s climate[1,2,3]

  • BUSCO analysis showed a high degree of completeness of the genome, with 282 out of 303 (93.1%) complete eukaryotic universal genes (Supplementary Table 1)

  • We suggest that P. coloniale retained the kynurenine pathway, not for Nicotinamide adenine dinucleotide (NAD) synthesis but for synthesis of picolinic acid

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Summary

Introduction

One of the most important biological events in the history of life was the successful colonization of the terrestrial landscape by green plants (Viridiplantae) that paved the way for terrestrial animal evolution, altering geomorphology and changes in the Earth’s climate[1,2,3]. While the majority of the early-diverging lineages in the Chlorophyta consisted of (mostly marine) scaly flagellates, some lineages were represented by very small, non-flagellate unicells often surrounded by cell walls[23,24]. One of these lineages, provisionally termed ‘Prasinococcales’[23] (clade VI), could not be reliably positioned in phylogenetic trees[24,25]. The genome of P. coloniale provided new insights into pico-eukaryotic biology near the dawn of green plant evolution

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