A Phylogenomic Framework to Study the Diversity and Evolution of Stramenopiles (=Heterokonts)

Abstract

Stramenopiles or heterokonts constitute one of the most speciose and diverse clades of protists. It includes ecologically important algae (such as diatoms or large multicellular brown seaweeds), as well as heterotrophic (e.g. bicosoecids, MAST groups) and parasitic (e.g. Blastocystis, oomycetes) species. Despite their evolutionary and ecological relevance, deep phylogenetic relationships among stramenopile groups, inferred mostly from small-subunit (SSU) rDNA phylogenies, remain unresolved, especially for the heterotrophic taxa. Taking advantage of recently released stramenopile transcriptome and genome sequences, as well as data from the genomic assembly of the MAST-3 species Incisomonas marina generated in our laboratory, we have carried out the first extensive phylogenomic analysis of stramenopiles, including representatives of most major lineages. Our analyses, based on a large dataset of 339 widely distributed proteins, strongly support a root of stramenopiles lying between two clades, Bigyra and Gyrista (Pseudofungi plus Ochrophyta). Additionally, our analyses challenge the Phaeista-Khakista dichotomy of photosynthetic stramenopiles (ochrophytes) as two groups previously considered to be part of the Phaeista (Pelagophyceae and Dictyochophyceae), branch with strong support with the Khakista (Bolidophyceae and Diatomeae). We propose a new classification of ochrophytes within the two groups Chrysista and Diatomista to reflect the new phylogenomic results. Our stramenopile phylogeny provides a robust phylogenetic framework to investigate the evolution and diversification of this group of ecologically relevant protists.

Competition between Silicifiers and Non-silicifiers in the Past and Present Ocean and Its Evolutionary Impacts

“…In this scenario, the diatom SITs arose from a single gene duplication and fusion event that also gave rise to the haptophyte and loricate choanoflagellate SITs, and must have occurred early in eukaryotic evolution, before these groups diverged deep in the Precambrian (Parfrey et al, 2011). The phylogenetic signal supports the scenario that the other stramenopile SITs arose from at least two other duplication-fusion events within the ochrophyte stramenopile clade itself, but after diatoms diverged, potentially as recently as the Mesozoic (Brown and Sorhannus, 2010;Derelle et al, 2016). It is hypothesized that this is a remarkable case of convergent molecular evolution, and that the independent invention of SITs from SIT-Ls was in response to competition for silicic acid from the rise of the diatoms after the Jurassic period (Marron et al, 2016b).…”

Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome

“…These origins were grouped into six evolutionary categories, red algae, green algae, aplastidic stramenopiles, other eukaryotes, prokaryotes, and viruses (Figure 3, panel A).

10.7554/eLife.23717.014Figure 3.Evolutionary origins of the ochrophyte plastid proteome.(Panel A ) displays the origins inferred by BLAST top hit, phylogenetic analysis, and combined analysis for all ancestral HPPGs. (Panel B ) shows (i) a schematic diagram of stramenopile taxonomy, with the evolutionary relationships between labyrinthulomycetes, oomycetes, slopalinids and ochrophytes proposed by recent multigene studies (Derelle et al, 2016), and the probable closest stramenopile relative (as inferred by BLAST top hit analysis) of the 26 ancestral HPPGs verified by combined analysis to be of aplastidic stramenopile origin, and (ii) the next nearest relative, as inferred through BLAST top hit, phylogenetic and combined analysis, of the 26 aplastidic stramenopile HPPGs verified by combined analysis. The evolutionary categories in this graph are shaded as per in panel A. DOI: http://dx.doi.org/10.7554/eLife.23717.014

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“…Because oomycetes are the sister-group of ochrophytes (Aleoshin et al, 2016; Derelle et al, 2016), this suggests that our dataset retains useful phylogenetic signal.…”

“…The ochrophytes include the diatoms, which are major primary producers in the ocean (Bowler et al, 2010; Armbrust et al, 2004), multicellular kelps, which serve as spawning grounds for marine animals (Cock et al, 2010) and the pelagophytes, microscopic algae of which some are known to form harmful blooms (Gobler et al, 2011) (Figure 1, panel A; Figure 1—figure supplement 1). The stramenopiles also contain many aplastidic and non-photosynthetic lineages (e.g., oomycetes), which diverge at the base of the ochrophytes and play important roles as pathogens and in microbial food webs (Aleoshin et al, 2016; Derelle et al, 2016) (Figure 1—figure supplement 1).

10.7554/eLife.23717.003Figure 1.Procedure for identification of conserved plastid-targeted proteins in ochrophytes.(Panel A ) shows a schematic unrooted ochrophyte tree, with the three major ochrophyte lineages (chrysista, hypogyristea, and diatoms) denoted by different coloured labels.

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Ferredoxin-dependent bilin reductases in eukaryotic algae: Ubiquity and diversity

“…Together with alveolates and rhizarians, they form a monophyletic assemblage known as the SAR clade (Burki et al, 2016). A stramenopile clade, the Ochrophyta, is proposed to include all photosynthetic species (Derelle et al, 2016; Sevcikova et al, 2015). Such ochrophytes acquired photosynthesis via endosymbiosis of a eukaryotic rhodophyte alga.…”