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New Phylogenomic Analysis of the Enigmatic Phylum Telonemia Further Resolves the Eukaryote Tree of Life Article Open Access

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New Phylogenomic Analysis of the Enigmatic Phylum Telonemia Further Resolves the Eukaryote Tree of Life Article Open Access New Phylogenomic Analysis of the Enigmatic Phylum Telonemia Further Resolves the Eukaryote Tree of Life Ju¨rgen F.H. Strassert,1 Mahwash Jamy,1 Alexander P. Mylnikov,2 Denis V. Tikhonenkov,2 and Fabien Burki*,1,3 1Department of Organismal Biology, Program in Systematic Biology, Uppsala University, Uppsala, Sweden 2Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Yaroslavl Region, Russia 3Science for Life Laboratory, Uppsala University, Uppsala, Sweden *Corresponding author: E-mail: [email protected]. Associate Editor: Beth Shapiro Abstract The resolution of the broad-scale tree of eukaryotes is constantly improving, but the evolutionary origin of several major groups remains unknown. Resolving the phylogenetic position of these “orphan” groups is important, especially those that originated early in evolution, because they represent missing evolutionary links between established groups. Telonemia is one such orphan taxon for which little is known. The group is composed of molecularly diverse biflagellated protists, often prevalent although not abundant in aquatic environments. Telonemia has been hypothesized to represent a deeply diverging eukaryotic phylum but no consensus exists as to where it is placed in the tree. Here, we established cultures and report the phylogenomic analyses of three new transcriptome data sets for divergent telonemid lineages. All our phylogenetic reconstructions, based on 248 genes and using site-heterogeneous mixture models, robustly resolve the evolutionary origin of Telonemia as sister to the Sar supergroup. This grouping remains well supported when as few as 60% of the genes are randomly subsampled, thus is not sensitive to the sets of genes used but requires a minimal alignment length to recover enough phylogenetic signal. Telonemia occupies a crucial position in the tree to examine the origin of Sar, one of the most lineage-rich eukaryote supergroups. We propose the moniker “TSAR” to accommodate this new mega-assemblage in the phylogeny of eukaryotes. Key words: TSAR, Telonemia, phylogenomics, eukaryotes, tree of life, protists. Introduction Thebackboneofthetreealsocontainsaseriesoflong- known and newly discovered enigmatic protist taxa that do The eukaryote tree of life is one of the oldest working hy- not fit within any established supergroup based on ultrastruc- potheses in biology. Over the past 15 years, this tree has been ture, ribosomal DNA phylogenies, or even protein-coding extensively reshaped based on phylogenomic studies of an genes (Brugerolle et al. 2002; Walker et al. 2006; Heiss et al. Article ever-increasing diversity of protists (i.e., microbial eukaryotes) 2011; Yabuki et al. 2012;seeAdl et al. 2018 for a more ex- (Burki et al. 2007; Rodriguez-Ezpeleta, Brinkmann, Burger, haustive list of incertae sedis taxa within eukaryotes). et al. 2007; Brown et al. 2013; Yabuki et al. 2014; Katz and Interestingly, phylogenomics suggested that many of these Grant 2015; Burki et al. 2016; Brown et al. 2018). The “orphan” taxa are themselves supergroup-level lineages, likely current tree places most lineages into a few redefined representing early diverging evolutionary intermediates be- “supergroups”—a taxonomic rank-less concept that was de- tween the established supergroups (Zhao et al. 2012; Brown vised as inclusive clades reasonably supported by molecular et al. 2013; Cavalier-Smith et al. 2015; Janouskovec et al. 2017; and/or morphological evidence (Simpson and Roger 2002, Heiss et al. 2018; Lax et al. 2018). Individual orphan lineages 2004; Keeling et al. 2005). As few as eight supergroups are can also turn out to be evolutionarily related, forming new recognized, sometimes arranged in even higher-order divi- larger deeply branching eukaryotic clade as in the case of the sions assuming the root of the tree falls outside of these recently proposed “CRuMs” supergroup (Brown et al. 2018). mega-clades: Diaphoretickes, including Sar, Haptista, Taken together, orphans can profoundly impact our under- Cryptista, Archaeplastida; Amorphea, including Amoebozoa standing of ancient eukaryote evolution by defining new ma- and Obazoa; Excavata, including Discoba and Metamonada jor branches in the tree and help establishing the branching (Burki 2014; Simpson et al. 2017; Adl et al. 2019). Importantly, pattern among all main eukaryotic groups. this view of the tree remains a working hypothesis and whilst The genus Telonema is one such orphan taxon that has most groups have been robustly and consistently supported, proven difficult to place in eukaryote-wide phylogenies. others have not and still await confirmation (this is mainly the Known for over a century, this genus contains only case for Archaeplastida and Excavata) (Burki et al. 2016; Heiss two named species, Telonema subtile (syn. Telonema et al. 2018). subtilis)andTelonema antarcticum (Griessmann 1913; ß The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] Open Access Mol. Biol. Evol. 36(4):757–765 doi:10.1093/molbev/msz012 Advance Access publication January 22, 2019 757 Strassert et al. doi:10.1093/molbev/msz012 MBE Klaveness et al. 2005). However, environmental sequencing of of available genomic data sets and the tentative placement of the 18S rDNA has shown that the genetic diversity of Telonemia in previous phylogenomic works (Burki et al. 2009, Telonema is relatively high in marine and freshwater environ- 2012, 2016), special attention was made to include represen- ments and in fact likely represent several genera (Shalchian- tatives of Diaphoretickes lineages with sufficient data. For the Tabrizi et al. 2007; Bra˚te et al. 2010; Adl et al. 2018). Telonema telonemids, at least two sequences from different data sets and related sequences are frequently detected in these were required to group together in gene trees in order to be aquatic environments, and although they are usually not retained. This requirement became possible by the addition very abundant, they are thought to play significant ecological of the new telonemid data sets and greatly lowered the risk roles as biflagellated heterotrophic predators of bacteria and that unidentified contaminants were wrongly assigned to small-sized eukaryotes (Klaveness et al. 2005). The ultrastruc- Telonemia. Overall, the sequence coverage for the three telo- ture of T. subtile and T. antarcticum revealed unique mor- nemid operational taxonomic units (OTUs) ranged between phological features, such as a multilayered subcortical lamina 58%and99%(supplementary table 1, Supplementary and complex cytoskeleton, that distinguish Telonema from all Material online), which constitutes a large improvement other eukaryotes (Klaveness et al. 2005; Shalchian-Tabrizi et al. over previous studies (e.g., Burki et al. 2016). Sequences cor- 2006; Yabuki et al. 2013). Yet, Telonema also possesses struc- responding to the bodonid prey Procryptobia sorokini, easily tures that are characteristics of other groups: for example, the identifiable in gene trees from the presence of other related peripheral vacuoles that are similar to the cortical alveoli in taxa (e.g., Neobodo designis, Bodo saltans), were reassigned Alveolata, tripartite tubular hairs on the long flagellum that accordingly. In total, 293 taxa were initially analyzed (supple- are similar to the mastigonemes in Stramenopila, or wheel- mentary fig. S1, Supplementary Material online), but this like structures resembling extrusomes in some Rhizaria number was reduced to 109 OTUs to allow computational- (Klaveness et al. 2005; Shalchian-Tabrizi et al. 2006; Yabuki heavy analyses. This final taxon sampling was selected based et al. 2013). This combination of unique and shared ultra- on the taxonomic affiliation and data coverage of the OTUs, structural features makes Telonema highly distinctive from excluding faster-evolving lineages when the selection of other eukaryotic groups and has supported the notion that shorter branches was possible (fig. 1, Supplementary fig. S1, it forms a phylum-level lineage—Telonemia—without close Supplementary Material online, and supplementary table 1, relatives (Shalchian-Tabrizi et al. 2006). Accordingly, the first Supplementary Material online). molecular phylogenies based on up to four genes provided only few clues as to the position of the group, other than it Tree Inference and Testing was not closely related to any known groups (Shalchian- The 248 genes/109 OTUs supermatrix was analyzed by max- Tabrizi et al. 2006). Later, more substantial analyses based imum likelihood (ML) and Bayesian tree reconstructions us- on larger data sets containing 127–351 genes also failed to ing site-heterogeneous mixture models of evolution, pinpoint with statistical significance the origin of Telonemia, specifically LGþC60þFþC4 with posterior mean site fre- but this was likely due at least in part to the small number of quency (PMSF) profiles and CATþGTRþC4, respectively genes sampled from only one species (T. subtile)(Burki et al. (see Materials and Methods). These models have been shown 2009, 2012, 2016; Lax et al. 2018). to be more robust against heterogeneity in the amino acid
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