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

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.

Proliferation of group II introns in the chloroplast genome of the green algaOedocladium carolinianum(Chlorophyceae)

“…Like the Chlorodendrophyceae, Pedinophyceae, Ulvophyceae and Trebouxiophyceae, this class is part of the core Chlorophyta, i.e., the rapid radiation of lineages that took place following the diversification of the prasinophyte algae. The precise relationships of the Chlorophyceae with the other core chlorophyte classes are still uncertain (Fucikova et al, 2014; Lemieux, Otis & Turmel, 2014; Leliaert & Lopez-Bautista, 2015; Sun et al, 2016; Turmel et al, 2016a). Five orders are currently recognized in the Chlorophyceae and as revealed by phylogenetic analyses of multiple chloroplast-encoded proteins/genes from representative taxa, they form two distinct clades: the CS clade consisting of the Chlamydomonadales (or Volvocales) and Sphaeropleales, and the OCC clade consisting of the Oedogoniales, Chaetophorales, and Chaetopeltidales (Turmel et al, 2008; Brouard et al, 2010; Lemieux et al, 2015; Watanabe et al, 2016).…”

Mitochondrial genomes of the green macroalga Ulva pertusa (Ulvophyceae, Chlorophyta): novel insights into the evolution of mitogenomes in the Ulvophyceae

“…, Smith and Keeling , Lemieux et al. ). The 95,880 bp Pseudendoclonium mtDNA was the first ulvophycean mitochondrial genome sequence reported with 57 genes and seven introns identified (Pombert et al.…”

Photosynthetic pigments of oceanic Chlorophyta belonging to prasinophytes clade VII

“…, Lemieux et al. ,b). The presence of astaxanthin as in core Chlorophyta while it is absent in other prasinophytes may reflect another common feature between clade VII and core Chlorophyta.…”