Common evolutionary origins of mechanosensitive ion channels in Archaea, Bacteria and cell-walled Eukarya

The ubiquity of mechanosensitive (MS) channels triggered a search for their functional homologs in Archaea. Archaeal MS channels were found to share a common ancestral origin with bacterial MS channels of large and small conductance, and sequence homology with several proteins that most likely function as MS ion channels in prokaryotic and eukaryotic cell-walled organisms. Although bacterial and archaeal MS channels differ in conductive and mechanosensitive properties, they share similar gating mechanisms triggered by mechanical force transmitted via the lipid bilayer. In this review, we suggest that MS channels of Archaea can bridge the evolutionary gap between bacterial and eukaryotic MS channels, and that MS channels of Bacteria, Archaea and cell-walled Eukarya may serve similar physiological functions and may have evolved to protect the fragile cellular membranes in these organisms from excessive dilation and rupture upon osmotic challenge.     

The origin of genes could be polyphyletic

The paradigm of the monophyletic origin of genes is deeply rooted in us all. For instance, this stems from the observation that the possibility of obtaining a good multiple alignment using the same protein from organisms from the three domains of life (Bacteria, Archaea and Eukarya) would seem to imply that the last universal common ancestor (LUCA) must have had that protein and, therefore, the origin of that gene must necessarily be monophyletic. The hypothesis of a polyphyletic origin of genes has to explain how it was possible to evolve highly conserved regions of multiple alignments of orthologous proteins from the three domains of life when these regions clearly seem to define a monophyletic origin of genes. If mRNAs were assembled at the stage of the LUCA through the trans-splicing of pieces of RNA representing mini-genes, and the translation of these mRNAs resulted in proteins whose genes (DNA) actually only evolved much later, i.e. only after the main domains of life were established, then this would explain why multiple alignments of orthologous proteins can be obtained from the three domains of life. Therefore, this makes these multiple alignments compatible with a polyphyletic origin of genes. I have analysed many multiple alignments of orthologous proteins from the three domains of life, reaching a conclusion that seems to suggest that these alignments are also compatible with a polyphyletic origin of genes because, for instance, they contain protein motifs characterising the domains of life. These motifs, and also genes, might have evolved late on, thus making their polyphyletic origin likely.     

Microbial radiation-resistance mechanisms

Organisms living in extreme environments have evolved a wide range of survival strategies by changing biochemical and physiological features depending on their biological niches. Interestingly, organisms exhibiting high radiation resistance have been discovered in the three domains of life (Bacteria, Archaea, and Eukarya), even though a naturally radiationintensive environment has not been found. To counteract the deleterious effects caused by radiation exposure, radiation- resistant organisms employ a series of defensive systems, such as changes in intracellular cation concentration, excellent DNA repair systems, and efficient enzymatic and non-enzymatic antioxidant systems. Here, we overview past and recent findings about radiation-resistance mechanisms in the three domains of life for potential usage of such radiationresistant microbes in the biotechnology industry.     

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.     

On How Many Fundamental Kinds of Cells are Present on Earth: Looking for Phylogenetic Traits that Would Allow the Identification of the Primary Lines of Descent

The phylogenetic analyses as far as the identification of the number of domains of life is concerned have not reached a clear conclusion. In the attempt to improve this circumstance, I introduce the concept that the amino acids codified in the genetic code might be of markers with outstanding phylogenetic power. In particular, I hypothesise the existence of a biosphere populated, for instance, by three groups of organisms having different genetic codes because codifying at least a different amino acid. Evidently, these amino acids would mark the proteins that are present in the three groups of organisms in an unambiguous way. Therefore, in essence, this mark would not be other than the one that we usually try to make in the phylogenetic analyses in which we transform the protein sequences in phylogenetic trees, for the purpose to identify, for example, the domains of life. Indeed, this mark would allow to classify proteins without performing phylogenetic analyses because proteins belonging to a group of organisms would be recognisable as marked in a natural way by at least a different amino acid among the diverse groups of organisms. This conceptualisation answers the question of how many fundamental kinds of cells have evolved from the Last Universal Common Ancestor (LUCA), as the genetic code has unique proprieties that make the codified amino acids excellent phylogenetic markers. The presence of the formyl-methionine only in proteins of bacteria would mark them and would identify these as domain of life. On the other hand, the presence of pyrrolysine in the genetic code of the euryarchaeota would identify them such as another fundamental kind of cell evolved from the LUCA. Overall, the phylogenetic distribution of formyl-methionine and pyrrolysine would identify at least two domains of life—Bacteria and Archaea—but their number might be actually four; that is to say, Bacteria, Euryarchaeota, archeobacteria that are not euryarchaeota and Eukarya. The usually accepted domains of life represented by Bacteria, Archaea and Eukarya are not compatible with the phylogenetic distribution of these two amino acids and therefore this last classification might be mistaken.     

Why Are There So Many Diverse Replication Machineries?

The replicon model has initiated a major research line in molecular biology: the study of DNA replication mechanisms. Until now, the majority of studies have focused on a limited set of model organisms, mainly from Bacteria or Opisthokont eukaryotes (human, yeasts) and a few viral systems. However, molecular evolutionists have shown that the living world is more complex and diverse than believed when the operon model was proposed. Comparison of DNA replication proteins in the three domains, Archaea, Bacteria, and Eukarya, have surprisingly revealed the existence of two distinct sets of non-homologous cellular DNA replication proteins, one in Bacteria and the other in Archaea and Eukarya, suggesting that the last universal common ancestor possibly still had an RNA genome. A major puzzle is the presence in eukaryotes of the unfaithful DNA polymerase alpha (Pol α) to prime Okazaki fragments. Interestingly, Pol α is specifically involved in telomere biosynthesis, and its absence in Archaea correlates with the absence of telomeres. The recent discovery of telomere-like GC quartets in eukaryotic replication origins suggests a link between Pol α and the overall organization of the eukaryotic chromosome. As previously proposed by Takemura, Pol α might have originated from a mobile element of viral origin that played a critical role in the emergence of the complex eukaryotic genomes. Notably, most large DNA viruses encode DNA replication proteins very divergent from their cellular counterparts. The diversity of viral replication machineries compared to cellular ones suggests that DNA and DNA replication mechanisms first originated and diversified in the ancient virosphere, possibly explaining why they are so many different types of replication machinerie.     

Evolution of arginine deiminase (ADI) pathway genes

We have analyzed the evolution of the three genes encoding structural enzymes of the arginine deiminase (ADI) pathway, arginine deiminase (ADI), ornithine transcarbamoylase (OTC), and carbamate kinase (CK) in a wide range of organisms, including Archaea, Bacteria, and Eukarya. This catabolic route was probably present in the last common ancestor to all the domains of life. The results obtained indicate that these genes have undergone a complex evolutionary history, including horizontal transfer events, duplications, and losses. Therefore, these genes are not adequate to infer organismal relationships at deep branching levels, but they provide an insight into how catabolic genes evolved and were assembled into metabolic pathways. Our results suggest that the three genes evolved independently and were later assembled into a single cluster with functional interdependence, thus, providing support for the gene recruitment hypothesis. Furthermore, the molecular phylogenetic analysis of OTC suggests a new classification of these genes into three subfamilies.     

The enigma of ribonuclease P evolution

The 5'-end maturation of tRNAs is catalyzed by the ribonucleoprotein enzyme ribonuclease P (RNase P) in all organisms. Here we provide, for the first time, a comprehensive overview on the representation of individual RNase P protein homologs within the Eukarya and Archaea. Most eukaryotes have homologs for all four protein subunits (Pop4, Rpp1, Pop5 and Rpr2) present in the majority of Archaea. Pop4 is the only RNase P protein subunit identifiable in all Eukarya and Archaea with available genome sequences. Remarkably, there is no structural homology between bacterial and archaeal-eukaryotic RNase P proteins. The simplest interpretation is that RNase P has an 'RNA-alone' origin and progenitors of Bacteria and Archaea diverged very early in evolution and then pursued completely different strategies in the recruitment of protein subunits during the transition from the 'RNA-alone' to the 'RNA-protein' state of the enzyme.     

Giant viruses coexisted with the cellular ancestors and represent a distinct supergroup along with superkingdoms Archaea, Bacteria and Eukarya

ABSTRACT: BACKGROUND: The discovery of giant viruses with genome and physical size comparable to cellular organisms, remnants of protein translation machinery and virus-specific parasites (virophages) have raised intriguing questions about their origin. Evidence advocates for their inclusion into global phylogenomic studies and their consideration as a distinct and ancient form of life. RESULTS: Here we reconstruct phylogenies describing the evolution of proteomes and protein domain structures of cellular organisms and double-stranded DNA viruses with medium-to-very-large proteomes (giant viruses). Trees of proteomes define viruses as a 'fourth supergroup' along with superkingdoms Archaea, Bacteria, and Eukarya. Trees of domains indicate they have evolved via massive and primordial reductive evolutionary processes. The distribution of domain structures suggests giant viruses harbor a significant number of protein domains including those with no cellular representation. The genomic and structural diversity embedded in the viral proteomes is comparable to the cellular proteomes of organisms with parasitic lifestyles. Since viral domains are widespread among cellular species, we propose that viruses mediate gene transfer between cells and crucially enhance biodiversity. CONCLUSIONS: Results call for a change in the way viruses are perceived. They likely represent a distinct form of life that either predated or coexisted with the last universal common ancestor (LUCA) and constitute a very crucial part of our planet's biosphere.     

Evolution of mitochondrial-type cytochrome c domains and of the protein machinery for their assembly

Proteins containing mitochondrial-type cytochrome c domains, defined here as protein domains having the mitochondrial cytochrome c fold, are found in organisms from all domains of life, and constitute essential components in several different metabolic pathways. The number of cytochrome c domains present in a given organism as well as their functional roles can vary widely even for quite closely related organisms. In this work, we have analysed in detail the distribution of mitochondrial-type cytochrome c domains along the tree of life and attempted to define the evolutionary relationships among them. In parallel, we have similarly analysed also the occurrence and distribution of the different machineries for cytochrome c assembly. It is found that the first appearance of mitochondrial-type cytochrome c domains has likely happened in the bacterial world, together with the first apparatus for their assembly. Evolution of cytochrome c domains has been extensive, involving several gene duplication and gene transfer events. Of particular relevance are gene transfer events from Bacteria to Eukarya and Archaea. The transfer of genes encoding cytochrome c domains has generally co-occurred with transfer of the assembly machinery. This has occurred also in Eukarya, where however the latter machinery has been subsequently replaced by a new one. It is possible that of the three known enzymatic systems for cytochrome c assembly, system II (found, among others, in cyanobacteria and Gram-positive bacteria) is the most ancient. Archaea have inherited from Bacteria system I or, possibly, an evolutionary intermediate between system II and system I.     

Climate sensitivity across marine domains of life: limits to evolutionary adaptation shape species interactions

Organisms in all domains, Archaea, Bacteria, and Eukarya will respond to climate change with differential vulnerabilities resulting in shifts in species distribution, coexistence, and interactions. The identification of unifying principles of organism functioning across all domains would facilitate a cause and effect understanding of such changes and their implications for ecosystem shifts. For example, the functional specialization of all organisms in limited temperature ranges leads us to ask for unifying functional reasons. Organisms also specialize in either anoxic or various oxygen ranges, with animals and plants depending on high oxygen levels. Here, we identify thermal ranges, heat limits of growth, and critically low (hypoxic) oxygen concentrations as proxies of tolerance in a meta‐analysis of data available for marine organisms, with special reference to domain‐specific limits. For an explanation of the patterns and differences observed, we define and quantify a proxy for organismic complexity across species from all domains. Rising complexity causes heat (and hypoxia) tolerances to decrease from Archaea to Bacteria to uni‐ and then multicellular Eukarya. Within and across domains, taxon‐specific tolerance limits likely reflect ultimate evolutionary limits of its species to acclimatization and adaptation. We hypothesize that rising taxon‐specific complexities in structure and function constrain organisms to narrower environmental ranges. Low complexity as in Archaea and some Bacteria provide life options in extreme environments. In the warmest oceans, temperature maxima reach and will surpass the permanent limits to the existence of multicellular animals, plants and unicellular phytoplankter. Smaller, less complex unicellular Eukarya, Bacteria, and Archaea will thus benefit and predominate even more in a future, warmer, and hypoxic ocean.     

Bacterial tyrosine kinases: evolution, biological function and structural insights

Reversible protein phosphorylation is a major mechanism in the regulation of fundamental signalling events in all living organisms. Bacteria have been shown to possess a versatile repertoire of protein kinases, including histidine and aspartic acid kinases, serine/threonine kinases, and more recently tyrosine and arginine kinases. Tyrosine phosphorylation is today recognized as a key regulatory device of bacterial physiology, linked to exopolysaccharide production, virulence, stress response and DNA metabolism. However, bacteria have evolved tyrosine kinases that share no resemblance with their eukaryotic counterparts and are unique in exploiting the ATP/GTP-binding Walker motif to catalyse autophosphorylation and substrate phosphorylation on tyrosine. These enzymes, named BY-kinases (for Bacterial tYrosine kinases), have been identified in a majority of sequenced bacterial genomes, and to date no orthologues have been found in Eukarya. The aim of this review was to present the most recent knowledge about BY-kinases by focusing primarily on their evolutionary origin, structural and functional aspects, and emerging regulatory potential based on recent bacterial phosphoproteomic studies.     

Genomics and early cellular evolution. The origin of the DNA world.

The sequencing of several genomes from each of the three domains of life (Archaea, Bacteria and Eukarya) has provided a huge amount of data that can be used to gain insight about early cellular evolution. Some features of the universal tree of life based on rRNA polygenies have been confirmed, such as the division of the cellular living world into three domains. The monophyly of each domain is supported by comparative genomics. However, the hyperthermophilic nature of the 'last universal common ancestor' (LUCA) is not confirmed. Comparative genomics has revealed that gene transfers have been (and still are) very frequent in genome evolution. Nevertheless, a core of informational genes appears more resistant to transfer, testifying for a close relationship between archaeal and eukaryal informational processes. This observation can be explained either by a common unique history between Archaea and Eukarya or by an atypical evolution of these systems in Bacteria. At the moment, comparative genomics still does not allow to choose between a simple LUCA, possibly with an RNA genome, or a complex LUCA, with a DNA genome and informational mechanisms similar to those of Archaea and Eukarya. Further comparative studies on informational mechanisms in the three domains should help to resolve this critical question. The role of viruses in the origin and evolution of DNA genomes also appears an area worth of active investigations. I suggest here that DNA and DNA replication mechanisms appeared first in the virus world before being transferred into cellular organisms.     

Copper resistance determinants in bacteria.

Copper is an essential trace element that is utilized in a number of oxygenases and electron transport proteins, but it is also a highly toxic heavy metal, against which all organisms must protect themselves. Known bacterial determinants of copper resistance are plasmid-encoded. The mechanisms which confer resistance must be integrated with the normal metabolism of copper. Different bacteria have adopted diverse strategies for copper resistance, and this review outlines what is known about bacterial copper resistance mechanisms and their genetic regulation.     

Comparative genomic analyses of copper transporters and cuproproteomes reveal evolutionary dynamics of copper utilization and its link to oxygen

Copper is an essential trace element in many organisms and is utilized in all domains of life. It is often used as a cofactor of redox proteins, but is also a toxic metal ion. Intracellular copper must be carefully handled to prevent the formation of reactive oxygen species which pose a threat to DNA, lipids, and proteins. In this work, we examined patterns of copper utilization in prokaryotes by analyzing the occurrence of copper transporters and copper-containing proteins. Many organisms, including those that lack copper-dependent proteins, had copper exporters, likely to protect against copper ions that inadvertently enter the cell. We found that copper use is widespread among prokaryotes, but also identified several phyla that lack cuproproteins. This is in contrast to the use of other trace elements, such as selenium, which shows more scattered and reduced usage, yet larger selenoproteomes. Copper transporters had different patterns of occurrence than cuproproteins, suggesting that the pathways of copper utilization and copper detoxification are independent of each other. We present evidence that organisms living in oxygen-rich environments utilize copper, whereas the majority of anaerobic organisms do not. In addition, among copper users, cuproproteomes of aerobic organisms were larger than those of anaerobic organisms. Prokaryotic cuproproteomes were small and dominated by a single protein, cytochrome c oxidase. The data are consistent with the idea that proteins evolved to utilize copper following the oxygenation of the Earth.     

Nucleoid-associated proteins in Crenarchaea

Architectural proteins play an important role in compacting and organizing the chromosomal DNA in all three kingdoms of life (Eukarya, Bacteria and Archaea). These proteins are generally not conserved at the amino acid sequence level, but the mechanisms by which they modulate the genome do seem to be functionally conserved across kingdoms. On a generic level, architectural proteins can be classified based on their structural effect as DNA benders, DNA bridgers or DNA wrappers. Although chromatin organization in archaea has not been studied extensively, quite a number of architectural proteins have been identified. In the present paper, we summarize the knowledge currently available on these proteins in Crenarchaea. By the type of architectural proteins available, the crenarchaeal nucleoid shows similarities with that of Bacteria. It relies on the action of a large set of small, abundant and generally basic proteins to compact and organize their genome and to modulate its activity.     

The universal ancestor and the ancestors of Archaea and Bacteria were anaerobes whereas the ancestor of the Eukarya domain was an aerobe

The use of an oxyphobic index (OI) based on the propensity of amino acids to enter more frequently the proteins of anaerobes makes it possible to make inferences on the environment in which the last universal common ancestor (LUCA) lived. The reconstruction of the ancestral sequences of proteins using a method based on maximum likelihood and their attribution by means of the OI to the set of aerobe or anaerobe sequences has led to the following conclusions: the LUCA was an anaerobic 'organism', as were the ancestors of Archaea and Bacteria, whereas the ancestor of Eukarya was an aerobe. These observations seem to falsify the hypothesis that the LUCA was an aerobe and help to identify better the environment in which the first organisms lived.     

Copper and genomic stability in mammals

As the free ion and in the form of some complexes, there is no doubt that copper can promote damage to cellular molecules and structures through radical formation. At the same time, and perhaps as a consequence, mammals have evolved means of minimizing levels of free copper ions and destructive copper complexes that enter the organism and its cells. These means include tight binding of copper ions to protein carriers and transporters; direct exchange of copper between protein carriers, transporters, and cuproenzymes; and mobilization of secretory mechanisms and excretory pathways, as needed. As a consequence, normally, and except under certain genetic conditions, copper is likely to be benign to most mammals and not responsible for genomic instability, including fragmentation of and/or alterations to DNA, induction of mutations or apoptosis, or other toxic events. Indeed, cuproenzymes are important members of the antioxidant system of the organism.     

Origins of DNA replication in the three domains of life

Replication of DNA is essential for the propagation of life. It is somewhat surprising then that, despite the vital nature of this process, cellular organisms show a great deal of variety in the mechanisms that they employ to ensure appropriate genome duplication. This diversity is manifested along classical evolutionary lines, with distinct combinations of replicon architecture and replication proteins being found in the three domains of life: the Bacteria, the Eukarya and the Archaea. Furthermore, although there are mechanistic parallels, even within a given domain of life, the way origins of replication are defined shows remarkable variation.