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. 2018 Sep;255(5):1517-1574.
doi: 10.1007/s00709-018-1241-1. Epub 2018 Apr 17.

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

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Free PMC article

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

Thomas Cavalier-Smith et al. Protoplasma. .
Free PMC article

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; Cercozoa; Chromista; Harosa; Retaria; Rhizarian phylogeny.

Conflict of interest statement

The authors declare they have no conflict of interest.

Figures

Fig. 1
Fig. 1
PhyloBayes GTR-CAT-Γ tree of 159 eukaryote-wide taxa, excluding Plantae, using 187 proteins (50,964 amino acid positions). Black arrows show new rhizarian sequences and red arrows the two non-rhizarian sequences from two mixed cultures that we separated phylogenetically. Numbers after species names show how many amino acids were included for each. Most bipartitions had maximal support (1); posterior probabilities are only shown if they did not—in red for the only three for which both chains did not show this topology (max.diff. 1; 5735 trees summed for two chains after removing 1674 as burnin). On all figures, Rhizaria subgroup names reflect the revised Table 1 classification
Fig. 2
Fig. 2
PhyloBayes GTR-CAT-Γ consensus tree of 72 chromists using 187 proteins (50, 964 amino acid positions). Black arrows show new rhizarian sequences; the red arrow highlights Oxnerella, whose sequences were phylogenetically separated from Minimassisteria. Numbers after species names show how many amino acids were included for each. Most bipartitions had maximal support by both CAT and ML (1/100); support values are only shown for those that did not (posterior probabilities left; ML 100 fast bootstraps right). Dashes indicate bipartitions not found on the corresponding ML tree (Fig. S2). The two chains converged satisfactorily (maxdiff 0.244572; 25,345 trees summed after removing 14,399 as burnin)
Fig. 3
Fig. 3
187-protein PhyloBayes GTR-CAT-Γ tree for 75 chromists; those on Fig. 2 plus Rhogostoma, Microheliella and ‘Minchinia’ (blue arrow). Black arrows show new rhizarian sequences; the red arrow highlights Oxnerella, whose sequences were phylogenetically separated from Minimassisteria. Numbers after species names show how many amino acids were included for each (maximum possible 50,964). Most bipartitions had maximal support by both CAT and ML; support values are only shown for those that did not (posterior probabilities left; ML 100 fast bootstraps right); in red for those where the two summed chains gave conflicting topology (max. diff. 1; 3499 trees summed after removing 1016 as burn-in; as the text explains, a third chain agreed with this consensus topology for Cercozoa, with much stronger support (except for the incorrect position of Rhogostoma), but placed Ectoreta as sister to Endomyxa in agreement with Fig. 2). The corresponding ML tree is Fig. S3. Pp. pro parte (in part)
Fig. 4
Fig. 4
187-protein PhyloBayes GTR-CAT-Γ tree of 162 eukaryote-wide taxa, including short-branch glaucophytes to represent Plantae and ‘Minchinia’ (blue arrow). Black arrows show new rhizarian sequences and red arrows the two non-rhizarian sequences from the two mixed cultures that we separated phylogenetically. Numbers after species names show how many amino acids were included for each. Most bipartitions had maximal support on both chains; posterior probabilities are only shown if they did not—in red for those for which both chains did not show this topology (max. diff. 1); the tree shown is for chain 2 (3571 trees summed after removing 3148 as burn-in); in chain 1, Cryptista were rearranged, as in Cavalier-Smith et al. , with Microheliella forming a Corbihelia clade with Telonema and Picomonas (0.84 support) and Glaucophyta were weakly within Hacrobia (0.64, 0.56 support)
Fig. 5
Fig. 5
Summary of ordinal and subordinal relationships amongst Monadofilosa as shown by a site-heterogeneous tree for 317 18S rDNA sequences (complete tree is Fig. S12). Support values are posterior probabilities from Fig. S12 and on the right also for ML (Fig. S14) for the same alignment when exactly the same clades were present. Support values for terminal clades are to the right of their names. The position of Phaeodaria (excluded from these analyses in case their long branches artefactually attracted Cholamonas) is from the Rhizaria-wide analyses (Figs. S8–S11) where they were sister to Fiscullina irrespective of Cholamonas presence or absence
Fig. 6
Fig. 6
Body plan evolution in Rhizaria. The primary step in the evolution of Rhizaria from a Colponema-like harosan biciliate ancestor having cortical alveoli was argued to be a switch from planktonic to benthic feeding (Cavalier-Smith 2018) through origin of actin-supported filopodia for catching food instead of using ciliary currents to direct suspended prey into the feeding groove. This entailed de-emphasis of the ancestral excavate feeding groove, posterior ciliary vane loss, novel transition zone structures and subsequent divergence in two directions—yielding Cercozoa by evolving ciliary gliding and losing cortical alveoli; and Retaria by evolving larger cell size and filopodial anastomoses to form a non-ciliated trophic network of feeding reticulopodia and restriction of cilia to transient small-celled non-feeding gametes or zoospores. Early on, Retaria diverged into Endomyxa by losing cortical alveoli and Ectoreta by evolving new skeletons and much larger long-lived trophic cells that typically reproduce by multiple fission. Ectoreta probably first split to form the planktonic self-rowing Sticholonche that lost reticulopodia (not figured) and a reticulopodial ancestor of ancestrally benthic Foraminifera, emphasising feeding by granular reticulopodia supported by irregular microtubules and an extracellular test (and losing cortical alveoli), and planktonic Radiozoa with radiating food-trapping axopodia supported by geometrically regular microtubular axonemes. Radiozoa evolved two contrasting body plans: Polycystinea added dense material to the outer surface of cortical alveoli to form perforated central capsules separating the reticulose ectoplasm from the nucleus/mitochondria-containing endoplasm with its microtubule-nucleating axoplast (= centrosome) and evolved a radiating silica endoskeleton (for clarity not shown); their sisters (Acantharia, not figured) like Foraminifera lost alveoli but uniquely evolved a strontium sulphate endoskeleton associated with contractile myonemes and multiplied axoplasts (see text)
Fig. 7
Fig. 7
Dissimilar phylum-specific insertions in ribosomal protein L1 of rhizarian phyla Cercozoa and Retaria. All Cercozoa have homologous two-amino-acid insertions, whereas all Retaria have two separate non-homologous insertions (of one and three amino acids) at positions two amino acids apart. Sequences from GenBank or found by nucleotide BLAST against our and other transcriptomes or genomes and translation. Sequences for Guillardia and chlorarachneans are for cytoplasmic ribosomes and nuclear-coded—that for Guillardia in Burki et al. (2010) was misleadingly the periplastid nucleomorph-coded version and thus red algal in origin. In Burki et al. (2010) Fig. 8B, this region was misaligned and their transcriptome-derived ‘Reticulomyxa’ sequence was actually from a cercozoan contaminant (see text); that shown here is from the genome and has both authentic retarian signatures and thus likely genuinely from Reticulomyxa

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