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Multidomain Ribosomal Protein Trees and the Planctobacterial Origin of Neomura (Eukaryotes, Archaebacteria)

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Multidomain Ribosomal Protein Trees and the Planctobacterial Origin of Neomura (Eukaryotes, Archaebacteria) Protoplasma https://doi.org/10.1007/s00709-019-01442-7 REVIEW Multidomain ribosomal protein trees and the planctobacterial origin of neomura (eukaryotes, archaebacteria) Thomas Cavalier-Smith1 & Ema E-Yung Chao1 Received: 25 February 2019 /Accepted: 19 September 2019 # The Author(s) 2020 Abstract Palaeontologically, eubacteria are > 3× older than neomura (eukaryotes, archaebacteria). Cell biology contrasts ancestral eubac- terial murein peptidoglycan walls and derived neomuran N-linked glycoprotein coats/walls. Misinterpreting long stems connecting clade neomura to eubacteria on ribosomal sequence trees (plus misinterpreted protein paralogue trees) obscured this historical pattern. Universal multiprotein ribosomal protein (RP) trees, more accurate than rRNA trees, are taxonomically undersampled. To reduce contradictions with genically richer eukaryote trees and improve eubacterial phylogeny, we constructed site-heterogeneous and maximum-likelihood universal three-domain, two-domain, and single-domain trees for 143 eukaryotes (branching now congruent with 187-protein trees), 60 archaebacteria, and 151 taxonomically representative eubacteria, using 51 and 26 RPs. Site-heterogeneous trees greatly improve eubacterial phylogeny and higher classification, e.g. showing gracilicute monophyly, that many ‘rDNA-phyla’ belong in Proteobacteria, and reveal robust new phyla Synthermota and Aquithermota. Monoderm Posibacteria and Mollicutes (two separate wall losses) are both polyphyletic: multiple outer membrane losses in Endobacteria occurred separately from Actinobacteria; neither phylum is related to Chloroflexi, the most divergent prokaryotes, which originated photosynthesis (new model proposed). RP trees support an eozoan root for eukaryotes and are consistent with archaebacteria being their sisters and rooted between Filarchaeota (=Proteoarchaeota, including ‘Asgardia’) and Euryarchaeota sensu-lato (including ultrasimplified ‘DPANN’ whose long branches often distort trees). Two-domain trees group eukaryotes within Planctobacteria, and archaebacteria with Planctobacteria/Sphingobacteria. Integrated molecular/palaeontological evidence favours negibacterial ancestors for neomura and all life. Unique presence of key pre-neomuran characters favours Planctobacteria only as ancestral to neomura, which apparently arose by coevolutionary repercussions (explained here in detail, including RP replacement) of simultaneous outer membrane and murein loss. Planctobacterial C-1 methanotrophic enzymes are likely ances- tral to archaebacterial methanogenesis and β-propeller-α-solenoid proteins to eukaryotic vesicle coats, nuclear-pore-complexes, and intraciliary transport. Planctobacterial chaperone-independent 4/5-protofilament microtubules and MamK actin-ancestors prepared for eukaryote intracellular motility, mitosis, cytokinesis, and phagocytosis. We refute numerous wrong ideas about the universal tree. Keywords Ribosomal protein universal tree . Archaebacteria . Eubacterial phylogeny . Rooting eukaryote trees . Eukaryogenesis Introduction 1: the eubacteria-neomura dichotomy in cell structure Handling Editor: Peter Nick Use of ribosomal RNA sequences for phylogeny led to recog- Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00709-019-01442-7) contains supplementary nition of the important distinction between archaebacteria and material, which is available to authorized users. eubacteria (Fox et al. 1980). It soon became clear that archaebacteria are more closely related to eukaryotes than to * Thomas Cavalier-Smith eubacteria and that archaebacteria plus eukaryotes constitute a [email protected] clade characterised ancestrally by surface N-linked glycopro- teins. The archaebacteria/eukaryote clade was called neomura, 1 Department of Zoology, University of Oxford, South Parks Road, meaning new walls (Cavalier-Smith 1987c), to contrast it with Oxford OX1 3PS, UK eubacteria that typically have walls of murein peptidoglycan T. Cavalier-Smith, E. E.-Y. Chao a Fig. 1 Longstanding contradictory interpretations of the universal rRNA tree. On the ‘eubacteria-first’ view (a), eubacteria are the ancestral domain, several times older than neomura which arose by the neomuran revolution (Cavalier-Smith 1987c, 2002a), a radical cell transformation caused by loss of murein peptidoglycan by a eubacterium similarly to the origins of mycoplasmas and L-forms from Bacillia. a is strongly support- ed by the fossil record, which indicates that neomura are 3–4 times youn- ger (originating between 0.8 and 1.45 Ga, depending on controversial identification of fossils in this period as ‘stem eukaryotes’ or ‘unusually complex bacteria’: Cavalier-Smith 2006a). Associated changes in cell biology were explained in detail (Cavalier-Smith 2014) on the assump- tion that the eubacterial ancestor of neomura was a posibacterium (Lake et al. 2009; Valas and Bourne 2011), whereas new evidence presented here favours the more recent idea that it was a planctobacterium (Reynaud and Devos 2011). It argues that long stems at the base of neomura and eukaryotes on rDNA and RP trees result from episodic hyperacceleration of ribosome evolution caused by origins of cotranslational secretion of glycoproteins and the nucleus respectively (Cavalier-Smith 2002a). The ‘archaea ancient’ view (b) assumes that neomura are as old as eubacteria b and that neomuran and eubacterial characters evolved divergently imme- diately after the origin of life, often assuming that their membranes arose independently by simultaneous separate origins of acyl ester lipids in eubacterial ancestors and isoprenoid ethers in ancestral neomura (this ancient ‘lipid divide’ is now refuted by eubacterial prenyl ether lipids, and archaebacterial fatty acids). b is based on (1) highly dubious a priori ideas about archaebacteria (Woese and Fox 1977a, b); (2) the false as- sumption that rDNA nucleotide substitution rates have been largely un- changed since cells began; and (3) uncritical interpretation of the first protein paralogue trees that ignored the likelihood that they also are tem- porally distorted by episodic hyperacceleration causing long-branch arte- facts that misroot the three-domain tree in the stretched neomuran stem (Cavalier-Smith 2002a, 2006c). b imagined that eukaryotes replaced iso- prenoid ethers by α-proteobacterial acyl esters during mitochondrial en- slavement (Martin 1999). Variants of a and b exist that assume that archaebacteria are ancestral to, not sisters of, eukaryotes (Williams et al. 2013), but also accept neomura as a clade. In contrast, the prokaryotes- c late or eukaryotes-first (Mariscal and Doolittle 2015)view(c)assumes cells were originally eukaryote-like and prokaryotes arose by radical sim- plification (‘streamlining’:Forterre1995) but never explicitly attempted to explain how; Forterre (2013) now prefers b. Proponents of b and c ignore the fossil record that refutes both, and largely ignore cell biology, failing to explain how assumed cell transformations could have occurred (incredible for c; highly implausible selectively and mechanistically for b—yet b may still be the most widespread assumption despite its serious defects; many remain unaware that paralogue pairs more often favour a eubacterial root, like fossils). Only a offers a scientifically explicit hypothesis as to the cell structure of LUCA tree lying between them (Gogarten et al. 1989; Iwabe et al. (mycoplasmas that secondarily lost murein the sole exception) 1989); (c) neomura, specifically eukaryote-like cells, are an- instead of N-linked glycoproteins. From the outset, it was cestral to eubacteria, with the universal root lying within the controversial whether archaebacteria are ancestral to eukary- eukaryote stem or crown and prokaryotes having arisen by otes (Van Valen and Maiorana 1980; Williams et al. 2013)or secondary simplification (so called streamlining) (Forterre are their sisters (Cavalier-Smith 1987c, 2002a), still not un- 1995); Mariscal and Doolittle (2015) lumped 10 disparate ambiguously decided (Cavalier-Smith 2014). speculations as ‘eukaryote-first’, but all are extremely vague The cladistic relationship between eubacteria and neomura as to the overall cellular properties possessed by the last ‘uni- has been even more controversial, with three contrasting versal’ common ancestor of all life (LUCA), none explicit views (Fig. 1): (a) eubacteria are ancestral to neomura, which enough to be worthwhile scientific hypotheses about LUCA, are therefore younger (Cavalier-Smith 1987b, c, 2002a, 2014; and none truly eukaryote-first (i.e. none positing that LUCA Lake et al. 2009; Valas and Bourne 2011); (b) they are sisters had a nucleus, mitosis, meiosis, syngamy, ER-Golgi differen- and thus of roughly equal age, with the root of the universal tiated endomembrane system, and cilia or mitochondria, a Multidomain ribosomal protein trees and the planctobacterial origin of neomura (eukaryotes, archaebacteria) logical impossibility!) as they mostly refer only to relatively transfer from chloroplasts to archaebacteria (Petitjean et al. trivial mainly genomic molecular details and ignore most cell 2012) as explained later in this paper decisively shows that biology; calling them ‘eukaryote-first’ is conceptually mis- archaebacteria are at least three times younger than eubacteria, leading. Saying ‘eukaryote-first does not mean Eukarya first’ so the root must lie within eubacteria (Cavalier-Smith 2002a). was obscurantist. Unless we can confidently decide between
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