Hot crenarchaeal viruses reveal deep evolutionary connections

The discovery of archaeal viruses provides insights into the fundamental biochemistry and evolution of the Archaea. Recent studies have identified a wide diversity of archaeal viruses within the hot springs of Yellowstone National Park and other high-temperature environments worldwide. These viruses are often morphologically unique and code for genes with little similarity to other known genes in the biosphere, a characteristic that has complicated efforts to trace their evolutionary history. Comparative genomics combined with structural analysis indicate that spindle-shaped virus lineages might be unique to the Archaea, whereas other icosahedral viruses might share a common lineage with viruses of Bacteria and Eukarya. These studies provide insights into the evolutionary history of viruses in all three domains of life.     

Protein Ser/Thr/Tyr Phosphorylation in the Archaea

The third domain of life, the Archaea (formerly Archaebacteria), is populated by a physiologically diverse set of microorganisms, many of which reside at the ecological extremes of our global environment. Although ostensibly prokaryotic in morphology, the Archaea share much closer evolutionary ties with the Eukarya than with the superficially more similar Bacteria. Initial genomic, proteomic, and biochemical analyses have revealed the presence of “eukaryotic” protein kinases and phosphatases and an intriguing set of serine-, threonine-, and tyrosine-phosphorylated proteins in the Archaea that may offer new insights into this important regulatory mechanism.     

Cold stress response in Archaea

We live on a cold planet where more than 80% of the biosphere is permanently below 5°C, and yet comparatively little is known about the genetics and physiology of the microorganisms inhabiting these environments. Based on molecular probe and sequencing studies, it is clear that Archaea are numerically abundant in diverse low-temperature environments throughout the globe. In addition, non-low-temperature-adapted Archaea are commonly exposed to sudden decreases in temperature, as are other microorganisms, animals, and plants. Considering their ubiquity in nature, it is perhaps surprising to find that there is such a lack of knowledge regarding low-temperature adaptation mechanisms in Archaea, particularly in comparison to what is known about archaeal thermophiles and hyperthermophiles and responses to heat shock. This review covers what is presently known about adaptation to cold shock and growth at low temperature, with a particular focus on Antarctic Archaea. The review highlights the similarities and differences that exist between Archaea and Bacteria and eukaryotes, and addresses the potentially important role that protein synthesis plays in adaptation to the cold. By reviewing the present state of the field, a number of important areas for future research are identified. Received: August 10, 2000 / Accepted: September 26, 2000     

Homepeptide Repeats:Implications for Protein Structure,Function and Evolution

Analysis of protein sequences from Mycobacterium tuberculosis H37Rv(Mtb H37Rv) was performed to identify homopeptide repeatcontaining proteins(HRCPs).Functional annotation of the HRCPs showed that they are preferentially involved in cellular metabolism.Furthermore,these homopeptide repeats might play some specific roles in protein-protein interaction.Repeat length differences among Bacteria,Archaea and Eukaryotes were calculated in order to identify the conservation of the repeats in these divergent kingdoms.From the results,it was evident that these repeats have a higher degree of conservation in Bacteria and Archaea than in Eukaryotes.In addition,there seems to be a direct correlation between the repeat length difference and the degree of divergence between the species.Our study supports the hypothesis that the presence of homopeptide repeats influences the rate of evolution of the protein sequences in which they are embedded.Thus,homopeptide repeat may have structural,functional and evolutionary implications on proteins.     

Protein length in eukaryotic and prokaryotic proteomes

We analyzed length differences of eukaryotic, bacterial and archaeal proteins in relation to function, conservation and environmental factors. Comparing Eukaryotes and Prokaryotes, we found that the greater length of eukaryotic proteins is pervasive over all functional categories and involves the vast majority of protein families. The magnitude of these differences suggests that the evolution of eukaryotic proteins was influenced by processes of fusion of single-function proteins into extended multi-functional and multi-domain proteins. Comparing Bacteria and Archaea, we determined that the small but significant length difference observed between their proteins results from a combination of three factors: (i) bacterial proteomes include a greater proportion than archaeal proteomes of longer proteins involved in metabolism or cellular processes, (ii) within most functional classes, protein families unique to Bacteria are generally longer than protein families unique to Archaea and (iii) within the same protein family, homologs from Bacteria tend to be longer than the corresponding homologs from Archaea. These differences are interpreted with respect to evolutionary trends and prevailing environmental conditions within the two prokaryotic groups.     

The Evolution of Histidine Biosynthesis in Archaea: Insights into the <Emphasis Type="Italic">his</Emphasis> Genes Structure and Organization in LUCA

The available sequences of genes encoding the enzymes associated with histidine biosynthesis suggest that this is an ancient metabolic pathway that was assembled prior to the diversification of Bacteria, Archaea, and Eucarya. Paralogous duplication, gene elongation, and fusion events of several different his genes have played a major role in shaping this biosynthetic route. We have analyzed the structure and organization of histidine biosynthetic genes from 55 complete archaeal genomes and combined it with phylogenetic inference in order to investigate the mechanisms responsible for the assembly of the his pathway and the origin of his operons. We show that a wide variety of different organizations of his genes exists in Archaea and that some his genes or entire his (sub-)operons have been likely transferred horizontally between Archaea and Bacteria. However, we show that, in most Archaea, his genes are monofunctional (except for hisD) and scattered throughout the genome, suggesting that his operons might have been assembled multiple times during evolution and that in some cases they are the result of recent evolutionary events. An evolutionary model for the structure and organization of his genes in LUCA is proposed.     

Universal Sharing Patterns in Proteomes and Evolution of Protein Fold Architecture and Life

Protein evolution is imprinted in both the sequence and the structure of evolutionary building blocks known as protein domains. These domains share a common ancestry and can be unified into a comparatively small set of folding architectures, the protein folds. We have traced the distribution of protein folds between and within proteomes belonging to Eukarya, Archaea, and Bacteria along the branches of a universal phylogeny of protein architecture. This tree was reconstructed from global fold-usage statistics derived from a structural census of proteomes. We found that folds shared by the three organismal domains were placed almost exclusively at the base of the rooted tree and that there were marked heterogeneities in fold distribution and clear evolutionary patterns related to protein architecture and organismal diversification. These include a relative timing for the emergence of prokaryotes, congruent episodes of architectural loss and diversification in Archaea and Bacteria, and a late and quite massive rise of architectural novelties in Eukarya perhaps linked to multicellularity.Reviewing Editor : Dr. David Pollock     

Ribosomal protein-sequence block structure suggests complex prokaryotic evolution with implications for the origin of eukaryotes

Amino acid sequence alignments of orthologous ribosomal proteins found in Bacteria, Archaea, and Eukaryota display, relative to one another, an unusual segment or block structure, with major evolutionary implications. Within each of the prokaryotic phylodomains the sequences exhibit substantial similarity, but cross-domain alignments break up into (a) universal blocks (conserved in both phylodomains), (b) bacterial blocks (unalignable with any archaeal counterparts), and (c) archaeal blocks (unalignable with any bacterial counterparts). Sequences of those eukaryotic cytoplasmic riboproteins that have orthologs in both Bacteria and Archaea, exclusively match the archaeal block structure. The distinct blocks do not correlate consistently with any identifiable functional or structural feature including RNA and protein contacts. This phylodomain-specific block pattern also exists in a number of other proteins associated with protein synthesis, but not among enzymes of intermediary metabolism. While the universal blocks imply that modern Bacteria and Archaea (as defined by their translational machinery) clearly have had a common ancestor, the phylodomain-specific blocks imply that these two groups derive from single, phylodomain-specific types that came into existence at some point long after that common ancestor. The simplest explanation for this pattern would be a major evolutionary bottleneck, or other scenario that drastically limited the progenitors of modern prokaryotic diversity at a time considerably after the evolution of a fully functional translation apparatus. The vast range of habitats and metabolisms that prokaryotes occupy today would thus reflect divergent evolution after such a restricting event. Interestingly, phylogenetic analysis places the origin of eukaryotes at about the same time and shows a closer relationship of the eukaryotic ribosome-associated proteins to crenarchaeal rather than euryarchaeal counterparts.     

Global Patterns of Protein Domain Gain and Loss in Superkingdoms

Domains are modules within proteins that can fold and function independently and are evolutionarily conserved. Here we compared the usage and distribution of protein domain families in the free-living proteomes of Archaea, Bacteria and Eukarya and reconstructed species phylogenies while tracing the history of domain emergence and loss in proteomes. We show that both gains and losses of domains occurred frequently during proteome evolution. The rate of domain discovery increased approximately linearly in evolutionary time. Remarkably, gains generally outnumbered losses and the gain-to-loss ratios were much higher in akaryotes compared to eukaryotes. Functional annotations of domain families revealed that both Archaea and Bacteria gained and lost metabolic capabilities during the course of evolution while Eukarya acquired a number of diverse molecular functions including those involved in extracellular processes, immunological mechanisms, and cell regulation. Results also highlighted significant contemporary sharing of informational enzymes between Archaea and Eukarya and metabolic enzymes between Bacteria and Eukarya. Finally, the analysis provided useful insights into the evolution of species. The archaeal superkingdom appeared first in evolution by gradual loss of ancestral domains, bacterial lineages were the first to gain superkingdom-specific domains, and eukaryotes (likely) originated when an expanding proto-eukaryotic stem lineage gained organelles through endosymbiosis of already diversified bacterial lineages. The evolutionary dynamics of domain families in proteomes and the increasing number of domain gains is predicted to redefine the persistence strategies of organisms in superkingdoms, influence the make up of molecular functions, and enhance organismal complexity by the generation of new domain architectures. This dynamics highlights ongoing secondary evolutionary adaptations in akaryotic microbes, especially Archaea.     

Archaeal DNA replication and repair

Since the first archaeal genome was sequenced, much attention has been focused on the study of these unique microorganisms. We have learnt that although archaeal DNA metabolic processes (replication, recombination and repair) are more similar to the metabolic processes of Eukarya than those of Bacteria, Archaea are not simply 'mini Eukarya'. They are, in fact, a mosaic of the eukaryal and bacterial systems that also possess archaeal-specific features. Recent biochemical and structural studies of the proteins that participate in archaeal DNA replication and repair have increased our understanding of these processes.     

Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen.

Cytochrome oxidase is a key enzyme in aerobic metabolism. All the recorded eubacterial (domain Bacteria) and archaebacterial (Archaea) sequences of subunits 1 and 2 of this protein complex have been used for a comprehensive evolutionary analysis. The phylogenetic trees reveal several processes of gene duplication. Some of these are ancient, having occurred in the common ancestor of Bacteria and Archaea, whereas others have occurred in specific lines of Bacteria. We show that eubacterial quinol oxidase was derived from cytochrome c oxidase in Gram-positive bacteria and that archaebacterial quinol oxidase has an independent origin. A considerable amount of evidence suggests that Proteobacteria (Purple bacteria) acquired quinol oxidase through a lateral gene transfer from Gram-positive bacteria. The prevalent hypothesis that aerobic metabolism arose several times in evolution after oxygenic photosynthesis, is not sustained by two aspects of the molecular data. First, cytochrome oxidase was present in the common ancestor of Archaea and Bacteria whereas oxygenic photosynthesis appeared in Bacteria. Second, an extant cytochrome oxidase in nitrogen-fixing bacteria shows that aerobic metabolism is possible in an environment with a very low level of oxygen, such as the root nodules of leguminous plants. Therefore, we propose that aerobic metabolism in organisms with cytochrome oxidase has a monophyletic and ancient origin, prior to the appearance of eubacterial oxygenic photosynthetic organisms.     

Zelloberflächenstrukturen der Bacteria und Archaea

Cell wall types of Bacteria and Archaea The acaryote microorganisms are divided into the two domains Bacteria and Archaea. The third domain represent the Eukarya. There is no universal cell wall polymer found in all Bacteria and Archaea. Due to their morphology several cell wall types can be identified, but the chemical diversity of the individual polymers is considerably greater. Certain cell wall polymers are limited to one of the two domains of Bacteria or Archaea like the murein of the Bacteria or the pseudomurein of some methanogens. Peptidoglycans (murein, pseudomurein) do not occur in eukaryotes. On the other hand individual cell wall polymers possess similarities to polymers of other domains. The structural principle of the methanochondroitin is also implemented in the eukaryotic connective tissue. The cell wall polymers consist frequently of glycoconjugates in which the amino acid content (glycoproteins) or the glycan moiety (proteoglycan‐like polymers) predominate. Both components (carbohydrates, amino acids) can also occur in similar amounts (peptidoglycan). There exist also cell wall polymers, which consist only of glycans (slimes, methanochondroitin) or amino acids (proteins, poly‐γ‐D‐glutamyl polymers). Cell wall‐free species (Mycoplasma) also occur. The chemical composition of the cell surface polymers was one of the first phenotypic characteristics that supported the 16 sRNA concept of Carl Woese to assign acaryote organisms into the two domains Bacteria and Archaea. A common feature of all Archaea is the lack of muramic acid and an outer membrane. The later occurs in the gramnegative Bacteria. During the evolution of Bacteria and Archaea a great variety of chemically different cell wall polymers has been developed which allow the growth and interaction of Bacteria and Archaea in different habitats. In this paper, some important surface polymers of Bacteria and Archaea are presented according to their chemical composition.     

The archaellum: an old motility structure with a new name

Motility structures, called flagella, have been described in all three domains of life: Bacteria, Archaea and Eukarya. These structures are well studied in both Bacteria and Eukarya. However, already in eukaryotes there exists some confusion as to whether these structures should actually be called cilia. With increased studies conducted on organisms of the third domain of life, the Archaea, it has become clear that the archaeal flagellum only functionally appears similar to the bacterial flagellum, whereas it structurally resembles a bacterial type IV pilus. To resolve confusion due to unclear nomenclature, we propose renaming the archaeal flagellum as the 'archaellum'. This will make clear that the archaellum and the bacterial flagellum are two distinct structures that happen to both be used to enable microorganisms to swim.     

Genetic technologies for Archaea

Members of the third domain of life, the Archaea, possess structural, physiological, biochemical and genetic features distinct from Bacteria and Eukarya and, therefore, have drawn considerable scientific interest. Physiological, biochemical and molecular analyses have revealed many novel biological processes in these important prokaryotes. However, assessment of the function of genes in vivo through genetic analysis has lagged behind because suitable systems for the creation of mutants in most Archaea were established only in the past decade. Among the Archaea, sufficiently sophisticated genetic systems now exist for some thermophilic sulfur-metabolizing Archaea, halophilic Archaea and methanogenic Archaea. Recently, there have been developments in genetic analysis of thermophilic and methanogenic Archaea and in the use of genetics to study the physiology, metabolism and regulatory mechanisms that direct gene expression in response to changes of environmental conditions in these important microorganisms.     

About the last common ancestor, the universal life-tree and lateral gene transfer: a reappraisal

An organismal tree rooted in the bacterial branch and derived from a hyperthermophilic last common ancestor (LCA) is still widely assumed to represent the path followed by evolution from the most primeval cells to the three domains recognized among contemporary organisms: Bacteria, Archaea and Eucarya. In the past few years, however, more and more discrepancies between this pattern and individual protein trees have been brought to light. There has been an overall tendency to attribute these incongruities to widespread lateral gene transfer. However, recent developments, a reappraisal of earlier evidence and considerations of our own lead us to a quite different view. It would appear (i) that the role of lateral gene transfer was overemphasized in recent discussions of molecular phylogenies; (ii) that the LCA was probably a non-thermophilic protoeukaryote from which both Archaea and Bacteria emerged by reductive evolution but not as sister groups, in keeping with a current evolutionary scheme for the biosynthesis of membrane lipids; and (iii) that thermophilic Archaea may have been the first branch to diverge from the ancestral line.     

Microbial diversity in natural asphalts of the Rancho La Brea Tar Pits

Bacteria commonly inhabit subsurface oil reservoirs, but almost nothing is known yet about microorganisms that live in naturally occurring terrestrial oil seeps and natural asphalts that are comprised of highly recalcitrant petroleum hydrocarbons. Here we report the first survey of microbial diversity in ca. 28,000-year-old samples of natural asphalts from the Rancho La Brea Tar Pits in Los Angeles, CA. Microbiological studies included analyses of 16S rRNA gene sequences and DNA encoding aromatic ring-hydroxylating dioxygenases from two tar pits differing in chemical composition. Our results revealed a wide range of phylogenetic groups within the Archaea and Bacteria domains, in which individual taxonomic clusters were comprised of sets of closely related species within novel genera and families. Fluorescent staining of asphalt-soil particles using phylogenetic probes for Archaea, Bacteria, and Pseudomonas showed coexistence of mixed microbial communities at high cell densities. Genes encoding dioxygenases included three novel clusters of enzymes. The discovery of life in the tar pits provides an avenue for further studies of the evolution of enzymes and catabolic pathways for bacteria that have been exposed to complex hydrocarbons for millennia. These bacteria also should have application for industrial microbiology and bioremediation.     

Transcriptional regulation in Archaea

During the past few decades, it has become clear that microorganisms can thrive under the most diverse conditions, including extremes of temperature, pressure, salinity and pH. Most of these extremophilic organisms belong to the third domain of life, that of the Archaea. The organisms of this domain are of particular interest because most informational systems that are associated with archaeal genomes and their expression are reminiscent of those seen in Eucarya, whereas, most of their metabolic aspects are similar to those of Bacteria. A better understanding of the regulatory mechanisms of gene expression in Archaea will, therefore, help to integrate the body of knowledge regarding the regulatory mechanisms that underlie gene expression in all three domains of life.     

Translation initiation in Archaea: conserved and domain-specific features

Initiation is a critical step in translation, during which the ribosome lands on the start codon and sets the correct reading frame for mRNA decoding. The rate and efficiency of translation are largely determined by initiation, which is therefore the preferred target of translation regulation mechanisms. Initiation has incurred an extensive evolutionary divergence among the primary domains of cell descent. The Archaea, albeit prokaryotes, have an initiation mechanism and apparatus more complex than those of the Bacteria; the molecular details of archaeal initiation are just beginning to be unravelled. The most notable aspects of archaeal initiation are the presence of two, perhaps three, distinct mechanisms for mRNA-ribosome interaction and the presence of a relatively large set of IFs (initiation factors), several of which are shared exclusively with the Eukarya. Among these, the protein termed a/eIF2 (archaeal/eukaryotic IF2) and aIF6 (archaeal IF6) are of special interest, since they appear to play key regulatory roles in the Eukarya. Studies of the function of these factors in Archaea have uncovered new features that will help to elucidate their conserved and domain-specific functions.