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Multigene Phylogeny and Cell Evolution of Chromist Infrakingdom Rhizaria: Contrasting Cell Organisation of Sister Phyla Cercozoa and Retaria

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Multigene Phylogeny and Cell Evolution of Chromist Infrakingdom Rhizaria: Contrasting Cell Organisation of Sister Phyla Cercozoa and Retaria Protoplasma https://doi.org/10.1007/s00709-018-1241-1 ORIGINAL ARTICLE Multigene phylogeny and cell evolution of chromist infrakingdom Rhizaria: contrasting cell organisation of sister phyla Cercozoa and Retaria Thomas Cavalier-Smith1 & Ema E. Chao1 & Rhodri Lewis1 Received: 11 December 2017 /Accepted: 12 March 2018 # The Author(s) 2018 Abstract Infrakingdom Rhizaria is one of four major subgroups with distinct cell body plans that comprise eukaryotic kingdom Chromista. Unlike other chromists, Rhizaria are mostly heterotrophic flagellates, amoebae or amoeboflagellates, commonly with reticulose (net-like) or filose (thread-like) feeding pseudopodia; uniquely for eukaryotes, cilia have proximal ciliary transition-zone hub- lattices. They comprise predominantly flagellate phylum Cercozoa and reticulopodial phylum Retaria, whose exact phylogenetic relationship has been uncertain. Given even less clear relationships amongst cercozoan classes, we sequenced partial transcriptomes of seven Cercozoa representing five classes and endomyxan retarian Filoreta marina to establish 187-gene multiprotein phylogenies. Ectoreta (retarian infraphyla Foraminifera, Radiozoa) branch within classical Cercozoa as sister to reticulose Endomyxa. This supports recent transfer of subphylum Endomyxa from Cercozoa to Retaria alongside subphylum Ectoreta which embraces classical retarians where capsules or tests subdivide cells into organelle-containing endoplasm and anastomosing pseudopodial net-like ectoplasm. Cercozoa are more homogeneously filose, often with filose pseudopodia and/or posterior ciliary gliding motility: zooflagellate Helkesimastix and amoeboid Guttulinopsis form a strongly supported clade, order Helkesida. Cercomonads are polyphyletic (Cercomonadida sister to glissomonads; Paracercomonadida deeper). Thecofilosea are a clade, whereas Imbricatea may not be; Sarcomonadea may be paraphyletic. Helkesea and Metromonadea are successively deeper outgroups within cercozoan subphylum Monadofilosa; subphylum Reticulofilosa (paraphyletic on site-heterogeneous trees) branches earliest, Granofilosea before Chlorarachnea. Our multiprotein trees confirm that Rhizaria are sisters of infrakingdom Halvaria (Alveolata, Heterokonta) within chromist subkingdom Harosa (= SAR); they further support holophyly of chromist subkingdom Hacrobia, and are consistent with holophyly of Chromista as sister of kingdom Plantae. Site- heterogeneous rDNA trees group Kraken with environmental DNA clade ‘eSarcomonad’, not Paracercomonadida. Ectoretan fossil dates evidence ultrarapid episodic stem sequence evolution. We discuss early rhizarian cell evolution and multigene tree coevolutionary patterns, gene-paralogue evidence for chromist monophyly, and integrate this with fossil evidence for the age of Rhizaria and eukaryote cells, and revise rhizarian classification. Keywords Cell evolution . Chromista . Harosa . Rhizarian phylogeny . Cercozoa . Retaria Introduction Handling Editor: Peter Nick Eukaryotes are classified in five kingdoms: unicellular, largely Electronic supplementary material The online version of this article phagotrophic Protozoa are ancestors of four biologically very (https://doi.org/10.1007/s00709-018-1241-1) contains supplementary — material, which is available to authorized users. distinct clades osmotrophic Fungi, epithelial phagotrophic Animalia, photosynthetic Plantae and Chromista (Cavalier- * Thomas Cavalier-Smith Smith 1998a, 2018; Ruggiero et al. 2015). Animalia and tom.cavalier–[email protected] Fungi are all heterotrophs. Almost all Plantae are photosyn- thetic. Their arguably sister kingdom Chromista includes all 1 Department of Zoology, University of Oxford, South Parks Road, chromophyte algae (e.g. diatoms, brown algae, dinoflagel- Oxford OX1 3PS, UK lates, haptophytes), as well as some major heterotrophic T. Cavalier-Smith et al. protist groups, notably ciliates, sporozoa, heterotrophic Smith et al. 2004; Burki et al. 2010;Sierraetal.2013,109- heterokonts, heliozoans, and the largely non-photosynthetic gene analysis). However, improved rhizarian gene and taxon infrakingdom Rhizaria, the subject of this paper. The predato- sampling for multiprotein trees and use of evolutionarily more ry lifestyle of Rhizaria and details of motility, cell ultrastruc- realistic site-heterogeneous algorithms (Cavalier-Smith et al. ture, and body form differ radically from those familiar to cell 2015a; Krabberød et al. 2017) yielded a consensus that biologists focusing on animal, fungal or plant cells. Endomyxa and revised Retaria and Cercozoa (Cavalier- Rhizaria are characterised by (1) having an ultrastructurally Smith 2018) are all clades. Multiprotein trees robustly support unique ciliary transition zone [Cavalier-Smith and Karpov monophyly of Rhizaria, always a strongly supported clade 2012b; earlier Cavalier-Smith et al. (2008, 2009) incorrectly (Burki et al. 2007, 2008, 2009, 2010, 2012; Cavalier-Smith thought the transitional proximal hub-lattice and distal hub- et al. 2014, 2015a; Krabberød et al. 2017). spoke structures were restricted to classical Cercozoa] and (2) Cercozoa are now recognised as ancestrally biciliate hetero- the widespread presence of reticulose (net-like) or filose trophic flagellates that typically glide on the posterior cilium (thread-like) feeding pseudopodia (Bass et al. 2009a). It is and have a marked propensity to form filose pseudopodia argued that the ciliary transition zone hub-lattice, hub-spoke (filopodia) for help in catching or ingesting prey (e.g. structure, and reticulose pseudopodia are three rhizarian syn- thaumatomonads); several times, some became filose amoebae apomorphies (Cavalier-Smith and Karpov 2012b), though it is by losing both cilia [often forming shell-like tests into which sometimes wrongly said they lack well-defined synapomor- they can withdraw pseudopodia for protection, e.g. Euglyphida, phies (e.g. Krabberød et al. 2017). Distinctiveness of rhizarian Lecythium, Penardeugenia (Dumack et al. 2016a, 2017b; cell biology is emphasised by novel features of actin, myosin Heger et al. 2010;Wylezichetal.2002)] or more rarely became and tubulin evolution with unique protein paralogues absent in planktonic flagellates by giving up the benthic gliding lifestyle other eukaryotes (Krabberød et al. 2017). [e.g. heterotrophic biciliate Katabia (Karpov et al. 2003); pho- As delimited by Cavalier-Smith (2003b), Rhizaria com- tosynthetic uniciliate Bigelowiella]. Cercozoa now comprise prise phyla Cercozoa (Cavalier-Smith 1998a, b)andRetaria two subphyla (Cavalier-Smith 2018): early diverging (Foraminifera plus Radiozoa: Cavalier-Smith 1999). A major Reticulofilosa (classes Chlorarachnea, Granofilosea, re-evaluation of kingdom Chromista adjusted the boundary Skiomonadea) and later evolving Monadofilosa (classes between Cercozoa and Retaria by transferring former Metromonadea, Helkesea, Sarcomonadea, Imbricatea, cercozoan subphylum Endomyxa to Retaria and establishing Thecofilosea). Unlike Retaria, reticulopodia are very rare in a new retarian subphylum Ectoreta to embrace Radiozoa and Cercozoa, apart from the strongly net-like granofilosean Foraminifera (Cavalier-Smith 2018); in doing so, Cercozoa Reticulamoeba (Bass et al. 2012), recently discovered scaly and Retaria became sister clades with contrasting cellular phe- Kraken (Dumack et al. 2016b, 2017a) and atypical net- notypes. That transfer was made for three reasons: (1) it forming meropodial Chlorarachnion. Filopodia predominate emphasised a primary divergence between often filose in five of the eight cercozoan classes, but are undetected in amoeboflagellates (Cercozoa) and non-flagellates with Metromonadea or Skiomonadea, and pseudopodia in amoeboid reticulose pseudopodia (Retaria); (2) 187-protein trees guttulinopsid Helkesea are mostly lobose (as they can be rarely (Cavalier-Smith et al. 2015a)stronglyshowedEndomyxaplus in sarcomonads or Thecofilosea). Apart from the strongly sup- Ectoreta as a clade (revised Retaria); and (3) it made Cercozoa ported deepest branching of the skiomonad Tremula on 18S phenotypically more uniform (ancestrally flagellates that rRNA trees (Howe et al. 2011a), the basal branching order of move by ciliary gliding on surfaces rather than swimming, a Cercozoa has always been poorly resolved on single-gene trees property never seen in Retaria). More recent 255-protein trees (Cavalier-Smith and Chao 2003a;Howeetal.2011a); demar- also robustly show Endomyxa, Ectoreta, revised Retaria and cation between Sarcomonadea and Imbricatea is particularly revised Cercozoa as clades (Krabberød et al. 2017), and thus unclear (Scoble and Cavalier-Smith 2014). fully support the transfer of Endomyxa to Retaria and formal Retaria ancestrally were trophically not flagellates but large restriction of Cercozoa to what used to be called ‘core amoeboid cells, usually with reticulose pseudopods Cercozoa’ (Nikolaev et al. 2004; Pawlowski 2008)orFilosa (reticulopodia) rather than filopodia; they form swimming (Cavalier-Smith 2003b, 2018). Many earlier sequence trees biciliate or uniciliate stages (never gliding) only transiently now appear to have been misleading with respect to relation- for dispersal or sexual reproduction and display a strong ten- ships of Endomyxa, Cercozoa and Ectoreta owing to insuffi- dency to cellular gigantism and evolution of mineral skeletons cient gene and taxon sampling. Thus some had placed either (Cavalier-Smith 2018). These skeletons, notably in foraminif- Foraminifera alone or Ectoreta as a whole within Endomyxa era (Payne
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