Multigene phylogeny and cell evolution of chromist infrakingdom Rhizaria: contrasting cell organisation of sister phyla Cercozoa and Retaria

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.Electronic supplementary materialThe online version of this article (10.1007/s00709-018-1241-1) contains supplementary material, which is available to authorized users.

Making sense of environmental sequencing data: Ecologically important functional traits of the protistan groups Cercozoa and Endomyxa (Rhizaria)

“…Our work is based on an extensive literature search. As a starting point, we used the classifications of Adl et al () and of Cavalier‐Smith et al (), and screened for functional traits only for taxa for which an 18S sequence was available.…”

“…The main taxonomic subdivisions are: (a) Endomyxa including Vampyrellida, Phytomyxea, Filoreta , Gromia and Ascetosporea (Bass et al, ; Sierra et al, ); (b) Cercozoa including the classes Sarcomonadea, Thecofilosea, Granofilosea, Imbricatea, Chlorarachnea and Metromonadea (Cavalier‐Smith et al, ); and (c) the incertae sedis rhizarian clades Aquavolonida, Tremulida and Novel Clade 12 (Bass et al, ).…”

“…Here we provide a functional database for Cercozoa and Endomyxa (sensu Cavalier‐Smith, Chao, & Lewis, ) to serve as a common reference and facilitate ecological studies. Increasing evidence from environmental sampling shows that these lineages are widespread and ubiquitous (de Vargas et al, ; Domonell, Brabender, Nitsche, Bonkowski, & Arndt, ; Fiore‐Donno et al, ; Geisen et al, ; Grossmann et al, ; Mahé et al, ; Turner et al, ; Urich et al, ).…”

Contrasting responses of protistan plant parasites and phagotrophs to ecosystems, land management and soil properties

“…Cercozoa (Cavalier-Smith, 1998), a highly diverse phylum of c. 600 described species (Pawlowski et al, 2012), is a major protistan lineage in soil (Geisen et al, 2015;Grossmann et al, 2016;Lanzén et al, 2016;Ferreira de Araujo et al, 2018), comprizing a vast array of functional traits in morphologies, nutrition and locomotion modes (Burki and Keeling, 2014). Recently the phylum Endomyxa was separated from Cercozoa Cavalier-Smith et al, 2018), and it is of particular interest for containing inter alia plant pathogens of functional and economic significance, including important transmitters of plant viruses and agents of root tumors (e.g. club root disease) (Neuhauser et al, 2014;Bass et al, 2019).…”

New phylogenomic analysis of the enigmatic phylum Telonemia further resolves the eukaryote tree of life

“…The eukaryote tree of life is one of the oldest working hypotheses in biology. Over the past 15 years, this tree has been extensively reshaped based on transcriptomic and genomic data for an ever-increasing diversity of protists (i.e., microbial eukaryotes), and the development of more realistic models of evolution Quang et al 2008;Yabuki et al 2014;Katz 2015;Burki et al 2016;Brown et al 2018;Cavalier-Smith et al 2018;Wang et al 2018). The current picture of the tree sees most lineages placed into a few redefined 'supergroups' -a taxonomic rank-less concept that was devised as inclusive clades reasonably supported by molecular and/or morphological evidence (Simpson and Roger 2002;Simpson and Roger 2004;Keeling et al 2005).…”