Large-Scale Phylogenomic Analyses Reveal That Two Enigmatic Protist Lineages, Telonemia and Centroheliozoa, Are Related to Photosynthetic Chromalveolates

Abstract

Understanding the early evolution and diversification of eukaryotes relies on a fully resolved phylogenetic tree. In recent years, most eukaryotic diversity has been assigned to six putative supergroups, but the evolutionary origin of a few major “orphan” lineages remains elusive. Two ecologically important orphan groups are the heterotrophic Telonemia and Centroheliozoa. Telonemids have been proposed to be related to the photosynthetic cryptomonads or stramenopiles and centrohelids to haptophytes, but molecular phylogenies have failed to provide strong support for any phylogenetic hypothesis. Here, we investigate the origins of Telonema subtilis (a telonemid) and Raphidiophrys contractilis (a centrohelid) by large-scale 454 pyrosequencing of cDNA libraries and including new genomic data from two cryptomonads (Guillardia theta and Plagioselmis nannoplanctica) and a haptophyte (Imantonia rotunda). We demonstrate that 454 sequencing of cDNA libraries is a powerful and fast method of sampling a high proportion of protist genes, which can yield ample information for phylogenomic studies. Our phylogenetic analyses of 127 genes from 72 species indicate that telonemids and centrohelids are members of an emerging major group of eukaryotes also comprising cryptomonads and haptophytes. Furthermore, this group is possibly closely related to the SAR clade comprising stramenopiles (heterokonts), alveolates, and Rhizaria. Our results link two additional heterotrophic lineages to the predominantly photosynthetic chromalveolate supergroup, providing a new framework for interpreting the evolution of eukaryotic cell structures and the diversification of plastids.

Large-scale phylogenomic analysis reveals the phylogenetic position of the problematic taxon Protocruzia and unravels the deep phylogenetic affinities of the ciliate lineages

“…This is the largest ''ciliate-based'' phylogenetic dataset assembled to date in terms of number of bases included. All previous studies were based either on single or a couple of genes or contained extremely limited sampling of ciliates (Bapteste et al, 2002;Brown et al, 2012;Budin and Philippe, 1998;Burki et al, 2009Burki et al, , 2013Greenwood et al, 1991;Hampl et al, 2009;Hammerschmidt et al, 1996;Katz et al, 2004;Lynn and Sogin, 1988;Sogin and Elwood, 1986).…”

“…Over the past few years, phylogenomic approaches have been employed to untangle deep relationships among major microbial eukaryotic lineages and place divergent taxa of evolutionary significance (Brown et al, 2012, in press;Burki et al, 2007Burki et al, , 2009Burki et al, , 2012Hampl et al, 2009;Parfrey et al, 2010;Zhao et al, 2012). Largescale phylogenomic analyses are now being utilized to resolve questions associated with the shallower nodes of the eukaryotic tree of life (Bachvaroff et al, 2011;Burki et al, 2010).…”

Phylogenomic analyses reveal subclass Scuticociliatia as the sister group of subclass Hymenostomatia within class Oligohymenophorea

“…Phylogenomic analyses that use omics data have generally improved the robustness of molecular phylogenetic reconstructions and untangled many previously debated phylogenies in various taxa (Brown et al, 2013;Burki et al, 2009;Burki et al, 2012;Burki et al, 2007;Feng et al, 2014).…”

Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree

“…In accord with my original intention that organisms demonstrated to have lost both characters should also be included in Chromista, I now place Alveolata, Rhizaria (phyla Cercozoa and Retaria) and centrohelid Heliozoa within Chromista (figure 1; electronic supplementary material, table S1), as multigene trees show that they belong to Chromista phylogenetically (Burki et al 2007(Burki et al , 2008(Burki et al , 2009Hackett et al 2007). Like chromists, photosynthetic dinoflagellates have chlorophyll c, but were originally excluded from Chromista because their ciliary hairs and membrane topology are simpler; their closest evolutionary affinities are with Ciliophora and Apicomplexa, grouped with them as protozoan infrakingdom Alveolata.…”