Multiple Origins of Heliozoa from Flagellate Ancestors
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Molecular Phylogenetics and Evolution 93 (2015) 331–362 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Multiple origins of Heliozoa from flagellate ancestors: New cryptist subphylum Corbihelia, superclass Corbistoma, and monophyly of Haptista, Cryptista, Hacrobia and Chromista q ⇑ Thomas Cavalier-Smith , Ema E. Chao, Rhodri Lewis Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK article info abstract Article history: Heliozoan protists have radiating cell projections (axopodia) supported by microtubular axonemes Received 7 April 2015 nucleated by the centrosome and bearing granule-like extrusomes for catching prey. To clarify previously Revised 25 June 2015 confused heliozoan phylogeny we sequenced partial transcriptomes of two tiny naked heliozoa, the Accepted 10 July 2015 endohelean Microheliella maris and centrohelid Oxnerella marina, and the cercozoan pseudoheliozoan Available online 31 July 2015 Minimassisteria diva. Phylogenetic analysis of 187 genes confirms that all are chromists; but centrohelids (microtubules arranged as hexagons and triangles) are not sisters to Endohelea having axonemes in Keywords: transnuclear cytoplasmic channels (triangular or square microtubular arrays). Centrohelids are strongly Cell evolution sister to haptophytes (together phylum Haptista); we explain the common origins of their axopodia and Chromista Haptista haptonema. Microheliella is sister to new superclass Corbistoma (zooflagellate Telonemea and Heliozoan phylogeny Picomonadea, with asymmetric microfilamentous pharyngeal basket), showing that these axopodial Picomonas protists evolved independently from zooflagellate ancestors. We group Corbistoma and Endohelea as Telonema new cryptist subphylum Corbihelia with dense fibrillar interorganellar connections; endohelean axopo- dia and Telonema cortex are ultrastructurally related. Differently sampled trees clarify why corticate multigene eukaryote phylogeny is problematic: long-branch artefacts probably distort deep multigene phylogeny of corticates (Plantae, Chromista); basal radiations may be contradictorily reconstructed because of their extreme closeness and the Bayesian star-tree paradox. Haptista and Hacrobia are holophyletic, and Chromista probably are. Ó 2015 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http:// creativecommons.org/licenses/by/4.0/). 1. Introduction strengthen the cell cortex of some subgroups (Cavalier-Smith, 2003a,b; Cavalier-Smith and Chao, 2003a). Chromista comprise Chromista include all eukaryotes with chloroplasts of secondary two subkingdoms: Harosa (Heterokonta, Alveolata, Rhizaria) and symbiogenetic red algal origin and all having tubular ciliary hairs, Hacrobia (Haptophyta, Cryptista, Heliozoa) (Cavalier-Smith, and thus most marine algae (e.g. brown algae, diatoms, 2010a). Their deepest phylogeny remains partially unclear and dinoflagellates, haptophytes) (Cavalier-Smith, 1981, 1986, 1989, controversial (Burki et al., 2012a; Keeling, 2013) as chromists 2007, 2010a). Chromists also include all descendants from that apparently underwent rapid evolutionary radiation near the time momentous red-algal enslavement (Cavalier-Smith, 2003a, of the symbiogenetic origin of chloroplasts (Cavalier-Smith, 2013a; Keeling, 2009) that later lost one or both characters, thus 2013a), essentially contemporaneously with basal branching of embrace many ecologically and evolutionarily important sec- Plantae, with which some chromist lineages therefore often inter- ondary heterotrophs, notably malarial and related parasites, mingle even on gene-rich phylogenetic trees (e.g. Brown et al., Pseudofungi, ciliates, disparate flagellates, and all axopodial pro- 2013; Burki et al., 2012a). A shared lateral gene transfer (LGT) from tists, e.g. Heliozoa (Yabuki et al., 2012), our focus here. Kingdoms bacteria into chloroplast DNA of haptophytes and cryptophytes Chromista and Plantae together form a clade known as corticates proved common ancestry of their chloroplasts (Rice and Palmer, because of their shared membrane-bounded alveoli that 2006), suggesting that Haptophyta are closer to cryptophytes than to heterokonts with which they were previously grouped as Chro- mophyta (Cavalier-Smith, 1981; after 1993 spelt Chromobiota). q This paper was edited by the Associate Editor J.B. Dacks. Some multigene trees show Hacrobia as a clade (Burki et al., ⇑ Corresponding author. 2009; Hackett et al., 2007; Patron et al., 2007; Janouškovec et al., E-mail address: [email protected] (T. Cavalier-Smith). http://dx.doi.org/10.1016/j.ympev.2015.07.004 1055-7903/Ó 2015 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). 332 T. Cavalier-Smith et al. / Molecular Phylogenetics and Evolution 93 (2015) 331–362 2010), but others (Baurain et al., 2010; Burki et al., 2012a) show data for Minimassisteria, discovered contaminating the O. marina paraphyletic Hacrobia, which would imply that this LGT was culture used for the RNA extraction (Howe et al., 2011). We report ancestral for all chromists but lost by Harosa (Cavalier-Smith, the phylogenetic position of all three using 187 genes from 171 2007), and an extended Chromobiota (i.e. Harosa, Haptophyta, eukaryotes. Microheliella, Telonema, and the previously phylogenet- Heliozoa) weakly holophyletic, with Cryptista more distant as clas- ically hard to place micropinocytotic zooflagellate Picomonas (Not sically assumed (Cavalier-Smith, 1982, 1986, 1989, 2000), but et al., 2007; Seenivasan et al., 2013) form a novel ancient hacrobian grouping with or within Plantae rather than with Harosa. Multi- chromist clade, here made a new cryptist subphylum Corbihelia gene trees disagree concerning the closest relatives of centrohelid because all three (alone in eukaryotes) share characteristic dense heliozoa (classified with haptophytes in Haptista: Cavalier-Smith, microfilamentous connections between mitochondria, nucleus, 2003b) and zooflagellate Telonemea (Shalchian-Tabrizi et al., endomembranes, and cytoskeleton, whose evolutionary signifi- 2006), classified in Cryptista (Cavalier-Smith, 2007), as they can cance was only recently recognised (Yabuki et al., 2012, 2013). This switch positions (Burki et al., 2009, 2012a,b). rules out four of the five previous mutually contradictory indica- Also uncertain is whether Chromista are holophyletic (as on tions of Picomonas relationships, with cryptomonads (Seenivasan 127-gene trees (Burki et al., 2009) and mitochondrial protein et al., 2013; Not et al., 2007), glaucophytes (Burki et al., 2012a), or 42-gene trees (Derelle and Lang, 2012; Zhao et al., 2013)), as classi- green plus red algae (Brown et al., 2013) and Haptista (Yabuki cally argued (Cavalier-Smith, 1986, 1989) and the simplest interpre- et al., 2014). As Picomonas and Telonema are sisters, as seen by tation, or polyphyletic as some multigene trees suggest (Baurain Not et al. (2007), Burki et al. (2013), and Yabuki et al. (2014), and et al., 2010; Burki et al., 2012a,b); apparent polyphyly might be an share a unique asymmetric microfilamentous cytopharyngeal bas- artefact of poor basal resolution amongst short-branch Hacrobia ket (Klaveness et al., 2005; Seenivasan et al., 2013) not known in and Plantae and longer harosan branches wrongly attracting Harosa any other eukaryotes, we group them as corbihelian superclass towards outgroups (Cavalier-Smith, 2009). If Chromista were poly- Corbistoma. As 18S rDNA first weakly suggested (Cavalier-Smith phyletic, sharing former red algal chloroplasts with the same novel and Chao, 2003b), centrohelid heliozoa are strongly sisters of protein-import machinery (Cavalier-Smith, 1999; Stork et al., 2012) haptophytes, confirming the holophyly of Haptista, an infraking- might in theory be attributed to serial tertiary transfers of dom established for haptophytes plus centrohelids only descendants of the singly enslaved red algal chloroplast from an (Cavalier-Smith, 2003b), here reduced in rank to phylum with hap- early cryptophyte to Haptophyta and from them to Harosa after tophytes and Centroheliozoa subphyla. We discuss evolution of the the first photosynthetic chromist evolved that new machinery cytopharynx and microtubule-supported cell extensions (axopodia (Cavalier-Smith et al., 1994; Baurain et al., 2010). Conversely, if and haptonema), alternative feeding modes within Hacrobia, and of chromists are holophyletic and ancestrally photophagotrophic, a tubular ciliary hairs shared by most cryptists, including at least one single red algal enslavement produced the ancestral chromist, sub- telonemid (Cavalier-Smith, 2007; Klaveness et al., 2005; Yabuki sequent plastid losses yielding ancestrally heterotrophic chromist et al., 2014), concluding that ultrastructure, multigene trees, and groups like ciliates, Rhizaria, and Heliozoa (Cavalier-Smith, 1999, shared LGT, together complementarily and convincingly demon- 2007, 2010a; Cavalier-Smith and Scoble, 2013). strate the holophyly and ancestral photophagotrophy of Hacrobia. Heliozoa are a subset of the many chromists with radial cellular Because of suspicions (Leigh et al., 2008; Deschamps and projections (axopodia) supported by an axoneme of interlinked Moreira, 2009) that corticate multigene phylogenies may be seri- microtubules in a geometrically regular array. Axopodia carry ously distorted by the dual evolutionary origin of chromists,