Chloroplast phylogenomic analysis resolves deep-level relationships within the green algal class Trebouxiophyceae

Claude Lemieux,Christian Otis,Monique Turmel

doi:10.1186/s12862-014-0211-2

Abstract

BackgroundThe green algae represent one of the most successful groups of photosynthetic eukaryotes, but compared to their land plant relatives, surprisingly little is known about their evolutionary history. This is in great part due to the difficulty of recognizing species diversity behind morphologically similar organisms. The Trebouxiophyceae is a species-rich class of the Chlorophyta that includes symbionts (e.g. lichenized algae) as well as free-living green algae. Members of this group display remarkable ecological variation, occurring in aquatic, terrestrial and aeroterrestrial environments. Because a reliable backbone phylogeny is essential to understand the evolutionary history of the Trebouxiophyceae, we sought to identify the relationships among the major trebouxiophycean lineages that have been previously recognized in nuclear-encoded 18S rRNA phylogenies. To this end, we used a chloroplast phylogenomic approach.ResultsWe determined the sequences of 29 chlorophyte chloroplast genomes and assembled amino acid and nucleotide data sets derived from 79 chloroplast genes of 61 chlorophytes, including 35 trebouxiophyceans. The amino acid- and nucleotide-based phylogenies inferred using maximum likelihood and Bayesian methods and various models of sequence evolution revealed essentially the same relationships for the trebouxiophyceans. Two major groups were identified: a strongly supported clade of 29 taxa (core trebouxiophyceans) that is sister to the Chlorophyceae + Ulvophyceae and a clade comprising the Chlorellales and Pedinophyceae that represents a basal divergence relative to the former group. The core trebouxiophyceans form a grade of strongly supported clades that include a novel lineage represented by the desert crust alga Pleurastrosarcina brevispinosa. The assemblage composed of the Oocystis and Geminella clades is the deepest divergence of the core trebouxiophyceans. Like most of the chlorellaleans, early-diverging core trebouxiophyceans are predominantly planktonic species, whereas core trebouxiophyceans occupying more derived lineages are mostly terrestrial or aeroterrestrial algae.ConclusionsOur phylogenomic study provides a solid foundation for addressing fundamental questions related to the biology and ecology of the Trebouxiophyceae. The inferred trees reveal that this class is not monophyletic; they offer new insights not only into the internal structure of the class but also into the lifestyle of its founding members and subsequent adaptations to changing environments.

Highlights

The green algae represent one of the most successful groups of photosynthetic eukaryotes, but compared to their land plant relatives, surprisingly little is known about their evolutionary history
These ultrastructural features, which apply to most green algae, supported the existence of the Streptophyta and Chlorophyta and revealed four distinct groups within the Chlorophyta that were recognized as classes: the predominantly marine, unicellular, Prasinophyceae; the predominantly marine and morphologically diverse Ulvophyceae; and the freshwater or terrestrial, morphologically diverse Trebouxiophyceae (=Pleurastrophyceae) and Chlorophyceae [5,6]
All data sets analyzed in our study were assembled from 79 chloroplast DNA (cpDNA)-encoded proteins and taxon sampling included up to 63 green algal taxa, i.e. the 38 trebouxiophyceans and pedinophyceans listed in Table 1, 23 additional chlorophytes (12 prasinophytes, nine chlorophyceans, and two ulvophyceans) and two streptophyte algae (Mesostigma viride and Chlorokybus atmophyticus)

Summary

Introduction

The green algae represent one of the most successful groups of photosynthetic eukaryotes, but compared to their land plant relatives, surprisingly little is known about their evolutionary history. Hypotheses on green algal phylogeny were based on morphology and ultrastructural data derived from the flagellar apparatus and processes of mitosis and cell division [3,4] These ultrastructural features, which apply to most green algae, supported the existence of the Streptophyta and Chlorophyta and revealed four distinct groups within the Chlorophyta that were recognized as classes: the predominantly marine, unicellular, Prasinophyceae; the predominantly marine and morphologically diverse Ulvophyceae; and the freshwater or terrestrial, morphologically diverse Trebouxiophyceae (=Pleurastrophyceae) and Chlorophyceae [5,6]. Phylogenetic analyses based on the nuclear-encoded small subunit rRNA gene (18S rDNA) largely corroborated these hypotheses [1,5,7] It was found, that the Prasinophyceae are paraphyletic, with the nine main lineages of prasinophytes identified so far representing the earliest branches of the Chlorophyta [8]. A recurrent theme that emerged from such studies is the finding that multiple genera containing taxa with reduced morphologies (such as unicells and filaments) are polyphyletic, with members often encompassing more than one class e.g. for Chlorella, [9,10]

Methods

Results

Discussion

Conclusion