Divergence Of Archaea Research Articles

ATP synthase evolution on a cross-braced dated tree of life

The timing of early cellular evolution, from the divergence of Archaea and Bacteria to the origin of eukaryotes, is poorly constrained. The ATP synthase complex is thought to have originated prior to the Last Universal Common Ancestor (LUCA) and analyses of ATP synthase genes, together with ribosomes, have played a key role in inferring and rooting the tree of life. We reconstruct the evolutionary history of ATP synthases using an expanded taxon sampling set and develop a phylogenetic cross-bracing approach, constraining equivalent speciation nodes to be contemporaneous, based on the phylogenetic imprint of endosymbioses and ancient gene duplications. This approach results in a highly resolved, dated species tree and establishes an absolute timeline for ATP synthase evolution. Our analyses show that the divergence of ATP synthase into F- and A/V-type lineages was a very early event in cellular evolution dating back to more than 4 Ga, potentially predating the diversification of Archaea and Bacteria. Our cross-braced, dated tree of life also provides insight into more recent evolutionary transitions including eukaryogenesis, showing that the eukaryotic nuclear and mitochondrial lineages diverged from their closest archaeal (2.67-2.19 Ga) and bacterial (2.58-2.12 Ga) relatives at approximately the same time, with a slightly longer nuclear stem-lineage.

The Ancient Origins of Death Domains Support the 'Original Sin' Hypothesis for the Evolution of Programmed Cell Death.

The discovery of caspase homologs in bacteria highlighted the relationship between programmed cell death (PCD) evolution and eukaryogenesis. However, the origin of PCD genes in prokaryotes themselves (bacteria and archaea) is poorly understood and a source of controversy. Whether archaea also contain C14 peptidase enzymes and other death domains is largely unknown because of a historical dearth of genomic data. Archaeal genomic databases have grown significantly in the last decade, which allowed us to perform a detailed comparative study of the evolutionary histories of PCD-related death domains in major archaeal phyla, including the deepest branching phyla of Candidatus Aenigmarchaeota, Candidatus Woesearchaeota, and Euryarchaeota. We identified death domains associated with executioners of PCD, like the caspase homologs of the C14 peptidase family, in 321 archaea sequences. Of these, 15.58% were metacaspase type I orthologues and 84.42% were orthocaspases. Maximum likelihood phylogenetic analyses revealed a scattered distribution of orthocaspases and metacaspases in deep-branching bacteria and archaea. The tree topology was incongruent with the prokaryote 16S phylogeny suggesting a common ancestry of PCD genes in prokaryotes and subsequent massive horizontal gene transfer coinciding with the divergence of archaea and bacteria. Previous arguments for the origin of PCD were philosophical in nature with two popular propositions being the "addiction" and 'original sin' hypotheses. Our data support the 'original sin' hypothesis, which argues for a pleiotropic origin of the PCD toolkit with pro-life and pro-death functions tracing back to the emergence of cellular life-the Last Universal Common Ancestor State.

Early Evolution of Transcription Systems and Divergence of Archaea and Bacteria.

DNA template-dependent multi-subunit RNA polymerases (RNAPs) found in all three domains of life and some viruses are of the two-double-Ψ-β-barrel (DPBB) type. The 2-DPBB protein format is also found in some RNA template-dependent RNAPs and a major replicative DNA template-dependent DNA polymerase (DNAP) from Archaea (PolD). The 2−DPBB family of RNAPs and DNAPs probably evolved prior to the last universal common cellular ancestor (LUCA). Archaeal Transcription Factor B (TFB) and bacterial σ factors include homologous strings of helix-turn-helix units. The consequences of TFB-σ homology are discussed in terms of the evolution of archaeal and bacterial core promoters. Domain-specific DPBB loop inserts functionally connect general transcription factors to the RNAP active site. Archaea appear to be more similar to LUCA than Bacteria. Evolution of bacterial σ factors from TFB appears to have driven divergence of Bacteria from Archaea, splitting the prokaryotic domains.

Why the Lipid Divide? Membrane Proteins as Drivers of the Split between the Lipids of the Three Domains of Life

Recent results from engineered and natural samples show that the starkly different lipids of archaea and bacteria can form stable hybrid membranes. But if the two types can mix, why don't they? That is, why do most bacteria and all eukaryotes have only typically bacterial lipids, and archaea archaeal lipids? It is suggested here that the reason may lie on the other main component of cellular membranes: membrane proteins, and their close adaptation to the lipids. Archaeal lipids in modern bacteria could suggest that the last universal common ancestor (LUCA) had both lipid types. However, this would imply a rather elaborate evolutionary scenario, while negating simpler alternatives. In light of widespread horizontal gene transfer across the prokaryotic domains, hybrid membranes reveal that the lipid divide did not just occur once at the divergence of archaea and bacteria from LUCA. Instead, it continues to occur actively to this day.

Histones predate the split between bacteria and archaea.

Histones form octameric complexes called nucleosomes, which organize the genomic DNA of eukaryotes into chromatin. Each nucleosome comprises two copies each of the histones H2A, H2B, H3 and H4, which share a common ancestry. Although histones were initially thought to be a eukaryotic innovation, the subsequent identification of archaeal homologs led to the notion that histones emerged before the divergence of archaea and eukaryotes. Here, we report the detection and classification of two new groups of histone homologs, which are present in both archaea and bacteria. Proteins in one group consist of two histone subunits welded into single-chain pseudodimers, whereas in the other they resemble eukaryotic core histone subunits and show sequence patterns characteristic of DNA binding. The sequences come from a broad spectrum of deeply-branching lineages, excluding their genesis by horizontal gene transfer. Our results extend the origin of histones to the last universal common ancestor. Supplementary data are available at Bioinformatics online.

Structural and mechanistic insights into the biosynthesis of CDP-archaeol in membranes.

The divergence of archaea, bacteria and eukaryotes was a fundamental step in evolution. One marker of this event is a major difference in membrane lipid chemistry between these kingdoms. Whereas the membranes of bacteria and eukaryotes primarily consist of straight fatty acids ester-bonded to glycerol-3-phosphate, archaeal phospholipids consist of isoprenoid chains ether-bonded to glycerol-1-phosphate. Notably, the mechanisms underlying the biosynthesis of these lipids remain elusive. Here, we report the structure of the CDP-archaeol synthase (CarS) of Aeropyrum pernix (ApCarS) in the CTP- and Mg2+-bound state at a resolution of 2.4 Å. The enzyme comprises a transmembrane domain with five helices and cytoplasmic loops that together form a large charged cavity providing a binding site for CTP. Identification of the binding location of CTP and Mg2+ enabled modeling of the specific lipophilic substrate-binding site, which was supported by site-directed mutagenesis, substrate-binding affinity analyses, and enzyme assays. We propose that archaeol binds within two hydrophobic membrane-embedded grooves formed by the flexible transmembrane helix 5 (TM5), together with TM1 and TM4. Collectively, structural comparisons and analyses, combined with functional studies, not only elucidated the mechanism governing the biosynthesis of phospholipids with ether-bonded isoprenoid chains by CTP transferase, but also provided insights into the evolution of this enzyme superfamily from archaea to bacteria and eukaryotes.

Chromatin is an ancient innovation conserved between Archaea and Eukarya

The eukaryotic nucleosome is the fundamental unit of chromatin, comprising a protein octamer that wraps ∼147 bp of DNA and has essential roles in DNA compaction, replication and gene expression. Nucleosomes and chromatin have historically been considered to be unique to eukaryotes, yet studies of select archaea have identified homologs of histone proteins that assemble into tetrameric nucleosomes. Here we report the first archaeal genome-wide nucleosome occupancy map, as observed in the halophile Haloferax volcanii. Nucleosome occupancy was compared with gene expression by compiling a comprehensive transcriptome of Hfx. volcanii. We found that archaeal transcripts possess hallmarks of eukaryotic chromatin structure: nucleosome-depleted regions at transcriptional start sites and conserved -1 and +1 promoter nucleosomes. Our observations demonstrate that histones and chromatin architecture evolved before the divergence of Archaea and Eukarya, suggesting that the fundamental role of chromatin in the regulation of gene expression is ancient.DOI:http://dx.doi.org/10.7554/eLife.00078.001.

The tripartite tricarboxylate transporter (TTT) family

Extracytoplasmic solute binding receptors are constituents of primary and secondary active transport systems. Previous studies have shown that the constituents of two such families (ABC and TRAP-T) occur in bacteria and archaea and have undergone minimal shuffling of constituents between systems during evolutionary history. We here show that a third family of binding receptor-dependent transporters, the tripartite tricarboxylate transporter (TTT) family, the prototype of which is the TctABC system of Salmonella typhimurium, occurs in many bacteria but not in archaea or eukaryotes. Phylogenetic analyses suggest that these systems have evolved from a primordial tripartite system with only two out of 39 possible examples of shuffling of constituents between systems. The occurrence of TctA homologues in many bacteria and archaea that apparently lack corresponding TctB and TctC homologues suggests that the appearance of tripartite systems was a relatively recent evolutionary invention that occurred after the divergence of archaea and eukaryotes from bacteria.

Common history at the origin of the position-function correlation in transcriptional regulators in archaea and bacteria.

Regulatory proteins in Escherichia coli with a helix-turn-helix (HTH) DNA binding motif show a position-function correlation such that repressors have this motif predominantly at the N terminus, whereas activators have the motif at the C-terminus extreme. Using this initial collection we identified by sequence comparison the exhaustive set of transcriptional regulators in 17 bacterial and 6 archaeal genomes. This enlarged set shows the same position-function correlation. The main question we address is whether this correlation is the result of common origin in evolution or the result of convergence. Evidence is presented supporting a common history at the origin of this correlation. We show the existence of a supergroup of eight repressor protein families sharing a conserved extended sequence comprising the classic HTH. Two of these repressor families (MarR and AsnC) originated before the divergence of Archaea and Bacteria. They are proposed at the origin of HTH-bearing transcriptional regulators currently present in Bacteria. The group of LysR proteins, with the HTH also at the N terminus, offers a control to the argument, since it shows clearly distinctive structural, functional, and evolutionary properties. This group of activator proteins, suggested to have originated within the Bacteria, has an advantageous gene organization to facilitate its horizontal transfer-used to conquer some Archaea-as well as negative autoregulation convenient for homeostasis, all of which agrees with this being the largest family in Bacteria. These results suggest that if shuffling of motifs occurred in Bacteria, it occurred only early in the history of these proteins, as opposed to what is observed in eukaryotic regulators.

Displacement of cellular proteins by functional analogues from plasmids or viruses could explain puzzling phylogenies of many DNA informational proteins

Comparative genomics has revealed many examples in which the same function is performed by unrelated or distantly related proteins in different cellular lineages. In some cases, this has been explained by the replacement of the original gene by a paralogue or non-homologue, a phenomenon known as non-orthologous gene displacement. Such gene displacement probably occurred early on in the history of proteins involved in DNA replication, repair, recombination and transcription (DNA informational proteins), i.e. just after the divergence of archaea, bacteria and eukarya from the last universal cellular ancestor (LUCA). This would explain why many DNA informational proteins are not orthologues between the three domains of life. However, in many cases, the origin of the displacing genes is obscure, as they do not even have detectable homologues in another domain. I suggest here that the original cellular DNA informational proteins have often been replaced by proteins of viral or plasmid origin. As viral and plasmid-encoded proteins are usually very divergent from their cellular counterparts, this would explain the puzzling phylogenies and distribution of many DNA informational proteins between the three domains of life.

A notable example of an evolutionary conserved gene: studies on a putative DNA helicase TIP49.

TIP49a (just called as simply TIP49 in previous reports [Kanemaki et al., 1997; Makino et al., 1998]) was found in a rat nuclear protein complex that included the TATA-binding protein. TIP49a possesses multiple sequence motifs for ATPase and DNA helicase. Since TIP49a structurally resembles prokaryotic DNA helicase RuvB, TIP49a is resumed to be a putative DNA helicase. We demonstrated TIP49a-related gene(s) in variety organisms from human to archaea. Amino acid identities expressed as aligned scores of human, yeast, and A. fulgidus TIP49a gene counterparts to the rat sequence were 99, 67, and 46, respectively. Strikingly, two homologous regions of mammalian TIP49a and bacterial RuvB exhibited an aligned score of 17-38. We demonstrated that the eukaryotic TIP49a counterparts were immunologically conserved. These lines of evidence show that the TIP49a gene is a notable example of a highly conserved gene among organisms. An extensive homology search revealed another class of TIP49-related gene in the eukaryotes, designated as TIP49b. Moreover, a phylogenetical study suggested that archaeal TIP49 genes belong to the TIP49b ancestor but not to the TIP49a one and that TIP49a evolved from TIP49b in accordance with divergence of archaea and eukarya. The TIP49 gene family is thought to play a fundamental role in a biological activity.

Ribosomal RNA precursor processing by a eukaryotic U3 small nucleolar RNA-like molecule in an archaeon

An RNA-containing endonuclease that catalyzes the excision and maturation of the 16S ribosomal RNA (rRNA) from the rRNA primary transcript (pre-rRNA) in the hyperthermophilic archaeon Sulfolobus acidocaldarius has been characterized. The ribonucleoprotein was inactivated by micrococcal nuclease treatment and inactivation was reversed by reconstitution with bulk RNA. A 159-nucleotide RNA with sequence and structural similarity to U3 small nucleolar RNAs of eukaryotes copurified with the endonuclease activity. Oligonucleotide-targeted ribonuclease H inactivation of the U3-like RNA component also abolished processing activity. A motif within the U3 homolog is complementary to the region around the three cleavage sites in the pre-RNA substrate. Thus, U3-mediated processing of pre-rRNA is not specific to eukaryotes; its origin predates the divergence of archaea and eukaryotes.