The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification.

Abstract

Prokaryotes constitute a single kingdom, Bacteria, here divided into two new subkingdoms : Negibacteria, with a cell envelope of two distinct genetic membranes, and Unibacteria, comprising the new phyla Archaebacteria and Posibacteria, with only one. Other new bacterial taxa are established in a revised higher-level classification that recognizes only eight phyla and 29 classes. Morphological, palaeontological and molecular data are integrated into a unified picture of large-scale bacterial cell evolution despite occasional lateral gene transfers. Archaebacteria and eukaryotes comprise the clade neomura, with many common characters, notably obligately co-translational secretion of N-linked glycoproteins, signal recognition particle with 7S RNA and translationarrest domain, protein-spliced tRNA introns, eight-subunit chaperonin, prefoldin, core histones, small nucleolar ribonucleoproteins (snoRNPs), exosomes and similar replication, repair, transcription and translation machinery. Eubacteria (posibacteria and negibacteria) are paraphyletic, neomura having arisen from Posibacteria within the new subphylum Actinobacteria (possibly from the new class Arabobacteria, from which eukaryotic cholesterol biosynthesis probably came). Replacement of eubacterial peptidoglycan by glycoproteins and adaptation to thermophily are the keys to neomuran origins. All 19 common neomuran character suites probably arose essentially simultaneously during the radical modification of an actinobacterium. At least 11 were arguably adaptations to thermophily. Most unique archaebacterial characters (prenyl ether lipids ; flagellar shaft of glycoprotein, not flagellin ; DNA-binding protein 10b ; specially modified tRNA ; absence of Hsp90) were subsequent secondary adaptations to hyperthermophily and/or hyperacidity. The insertional origin of protein-spliced tRNA introns and an insertion in proton-pumping ATPase also support the origin of neomura from eubacteria. Molecular co-evolution between histones and DNA-handling proteins, and in novel protein initiation and secretion machineries, caused quantum evolutionary shifts in their properties in stem neomura. Proteasomes probably arose in the immediate common ancestor of neomura and Actinobacteria. Major gene losses (e.g. peptidoglycan synthesis, hsp90, secA) and genomic reduction were central to the origin of archaebacteria. Ancestral archaebacteria were probably heterotrophic, anaerobic, sulphur-dependent hyperthermoacidophiles ; methanogenesis and halophily are secondarily derived. Multiple lateral gene transfers from eubacteria helped secondary archaebacterial adaptations to mesophily and genome re-expansion. The origin from a drastically altered actinobacterium of neomura, and the immediately subsequent simultaneous origins of archaebacteria and eukaryotes, are the most extreme and important cases of T. Cavalier-Smith quantum evolution since cells began. All three strikingly exemplify De Beer's principle of mosaic evolution : the fact that, during major evolutionary transformations, some org...

Description of 'Synergistetes' phyl. nov. and emended description of the phylum 'Deferribacteres' and of the family Syntrophomonadaceae, phylum 'Firmicutes'

“…Finally, the cell-wall structure, which was considered to be a character of high significance in bacterial evolution (Gupta, 1998;Cavalier-Smith, 2002), supported the argument for the paraphyly of the current family Syntrophomonadaceae. Current members of the family Syntrophomonadaceae other than those belonging to the 'Synergistes' clade also formed a deep-branched clade, but was supported by low bootstrap values.…”

Evolution of the cytoskeleton

“…Some archaea and mollicutes have no cell wall and already meet this requirement. The neomuran hypothesis (74) postulates that this might have occurred in bacteria. Second, the organism would need a mechanism for projecting the membrane in a manner that could engulf prey.…”

A microscopic model of evolution of recombination

“…The necessity to adapt to a hot acid environment led the common ancestor to lose the peptidoglican wall and develop the ability to synthesize membrane glycoproteins [8,6]. The eukaryotes that derived from the common ancestor were therefore characterized by a soft cell and a well-developed cytoskeleton and endomembrane system that made it easy to evolve phagotrophy.…”

“…According to Cavalier-Smith [5,6,7] the common ancestor of Eukaryotes and Archaebacteria was similar to the current Gram positive bacteria being surrounded by a cell membrane and a peptidoglican wall. The necessity to adapt to a hot acid environment led the common ancestor to lose the peptidoglican wall and develop the ability to synthesize membrane glycoproteins [8,6].…”