Multidomain ribosomal protein trees and the planctobacterial origin of neomura (eukaryotes, archaebacteria)

Abstract

Palaeontologically, eubacteria are > 3× older than neomura (eukaryotes, archaebacteria). Cell biology contrasts ancestral eubacterial 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 ancestral 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.

Cryo-Electron Tomography Reveals the Complex Ultrastructural Organization of Multicellular Filamentous Chloroflexota (Chloroflexi) Bacteria

“…For instance, lipopolysaccharides (LPS) have not been detected in C. aurantiacus and O. trichoides (Knudsen et al, 1982;Meissner et al, 1988;Keppen et al, 2018). Moreover, crucial genes of the LPS biosynthesis pathway have not been found in Chlorolexales or in other Chloroflexota species (Cavalier-Smith, 2006;Sutcliffe, 2010;Antunes et al, 2016;Keppen et al, 2018). In addition, we also analyzed Chloroflexota genomes, including the newly described "Ca.…”

“…The architecture of the multilayered cell envelope of Chloroflexota has been a source of debate for a long time. Among others, some points of contention have centered around some micrographs that arguably do not allow to undoubtedly determine discrete layers in the cell envelope ( Cavalier-Smith, 2006 ; Sutcliffe, 2011 ; Cavalier-Smith and Chao, 2020 ). Our tomograms revealed that both “ Ca .…”

“…The results presented here allow for a deeper understanding of the cell biology of Chloroflexales , as well as Chloroflexota bacteria in general. Particularly, these data provide new information to the debate surrounding the organization of the cell envelope in Chloroflexota ( Sutcliffe, 2011 ; Cavalier-Smith and Chao, 2020 ), the mechanism of their motility and adherence ( Fukushima et al, 2016 ; Fukushima, 2016 ), and finally on the multicellular organization of the phototrophic bacteria.…”

ToRQuEMaDA: tool for retrieving queried Eubacteria, metadata and dereplicating assemblies

“…The larger bacterial tree ( Fig. 5 ) results from an extremely aggressive selection ( Table 1 , B) but it still shows what we consider as the main groups of Bacteria (Proteobacteria, PVC, FBC, and “monoderm” phyla) and, after accounting for the idiosyncratic taxon names, most groups described by T. Cavalier-Smith ( Cavalier-smith & Chao, 2020 ) are visible (with the exception of Eoglycobacteria and Hadobacteria, which were both absorbed in polyphyletic groups). Regarding the topology of the tree, all the organisms from the main super-phyla are generally regrouped in the same subtree, with some exceptions.…”

ToRQuEMaDA: Tool for Retrieving Queried Eubacteria, Metadata and Dereplicating Assemblies

“…The larger bacterial tree ( Figure 5) results from an extremely aggressive selection ( Table 1, B) but it still shows what we consider as the main groups of Bacteria (Proteobacteria, PVC, FBC, and monoderms phyla) and, after accounting for the idiosyncratic taxon names, most groups described by T. Cavalier-Smith 41 are visible (with the exception of Eoglycobacteria and Hadobacteria, which were both absorbed in polyphyletic groups).…”