Ancestor Of Archaea Research Articles

The origins of the cell membrane, the progenote, and the universal ancestor (LUCA)

I analyse the consequences that the diversity of cell membranes present in bacteria and archaea would have for the stage reached by the evolution of cellularity in the Last Universal Common Ancestor (LUCA). Regardless of how the bacterial and archaeal membranes were distributed in the LUCA, the conclusion that would seem to emerge is always the same. That is to say, it is more likely that LUCA was a progenote rather than a genote. Indeed, if LUCA hosted both types of membranes then this would have been a transitional condition which would imply, in itself, that LUCA was a progenote. In other words, the two types of membranes evidently had to segregate in that of bacteria and that of archaea, and this segregation would imply enormous changes not expected for a cellular stage but the norm for that of progenote. Instead, in the case in which LUCA hosted only one type of membrane, for example that of archaea, then the evolution of the other type of membrane - presumably in the ancestor of bacteria - would imply a progenotic LUCA precisely because such a late origin would seem be an expression, at that time, of a still rapid and progressive evolution because it involves a fundamental and profound genetic trait, and should therefore reflect the progenotic stage. Finally, in the event that LUCA had been devoid of a membrane, then the late origin of the two types of membranes - in the ancestor of archaea and in that of bacteria - would seem to be a clear expression of a rapid and progressive evolution typical of progenote. Indeed, this would imply, for example, that all mechanisms and functions associated with the two cell membranes still had to evolve which would express the progenotic stage precisely because it would seem to be an evolution still in progress, and therefore typical of the stage of progenote. Therefore, LUCA was most likely a progenote also because there would be no strong arguments in favour of the hypothesis that LUCA had instead reached the evolutionary stage of cellularity.

Calpains in cyanobacteria and the origin of calpains

Calpains are cysteine proteases involved in many cellular processes. They are an ancient and large superfamily of enzymes responsible for the cleavage and irreversible modification of a large variety of substrates. They have been intensively studied in humans and other mammals, but information about calpains in bacteria is scarce. Calpains have not been found among Archaea to date. In this study, we have investigated the presence of calpains in selected cyanobacterial species using in silico analyses. We show that calpains defined by possessing CysPC core domain are present in cyanobacterial genera Anabaena, Aphanizomenon, Calothrix, Chamaesiphon, Fischerella, Microcystis, Scytonema and Trichormus. Based on in silico protein interaction analysis, we have predicted putative interaction partners for identified cyanobacterial calpains. The phylogenetic analysis including cyanobacterial, other bacterial and eukaryotic calpains divided bacterial and eukaryotic calpains into two separate monophyletic clusters. We propose two possible evolutionary scenarios to explain this tree topology: (1) the eukaryotic ancestor or an archaeal ancestor of eukaryotes obtained calpain gene from an unknown bacterial donor, or alternatively (2) calpain gene had been already present in the last common universal ancestor and subsequently lost by the ancestor of Archaea, but retained by the ancestor of Bacteria and by the ancestor of Eukarya. Both scenarios would require multiple independent losses of calpain genes in various bacteria and eukaryotes.

The RNase P, LUCA, the ancestors of the life domains, the progenote, and the tree of life

I have tried to interpret the phylogenetic distribution of the RNase P with the aim of helping to clarify the stage reached by the evolution of cellularity in the Last Universal Common Ancestor (LUCA); that is to say, if the evolutionary stage of the LUCA was represented by a protocell (progenote) or by a complete cell (genote). Since there are several arguments that lead one to believe that only the RNA moiety of the RNase P was present in the LUCA, this might imply that this evolutionary stage was actually the RNA world. If true this would imply that the LUCA was a progenote because the RNA world being a world subject to multiple evolutionary transitions that would involve a high noise at many its levels, which would fall within the definition of the progenote. Furthermore, since RNA-mediated catalysis is much less efficient than protein-mediated catalysis, then the only RNA moiety that was present in the LUCA could imply - by per se, without invoking the existence of the RNA world - that the LUCA was a progenote because an inefficient catalysis might have characterized this evolutionary stage. This evolutionary stage would still fall under the definition of the progenote. In addition, the observation that the protein moieties of the RNase P of bacteria and archaea are not-homologs would imply that these originated independently in the two main phyletic lineages. In turn, this would imply the progenotic nature of the ancestors of both archaea and bacteria. Indeed, it is admissible that such a late origin - in the main phyletic lineages - of the protein moieties of the RNase P is witness to an evolutionary transition towards a more efficient catalysis, evidently made clear precisely by the evolution of the protein moieties of the RNase P which would have helped the RNA of the RNase P to a more efficient catalysis. Hence, this would date that evolutionary moment as a transition to a much more efficient catalysis and consequently would imply which in that evolutionary stage there was the actual transition from the progenotic to genotic status. Finally, this late origin of the RNase P protein moieties in the bacterial and archaeal domains per se could imply the presence of a progenotic stage for their ancestors, or at least that a cell stage would have been much less likely. In fact, it is true that genes can originate both in a cellular and in a progenotic stage, but they mainly typify the latter because they are, by definition, in formation. Then it is expected that in the evolutionary stage of the formation of the main phyletic lineages - that is to say, in an evolutionary time in which the formation of genes might be expected - that the origin of proteins is to be related to a rapid and progressive evolution typical of the progenote precisely because in such an evolutionary stage the origin of genes is more easily and simply explained as reflecting a progenotic rather than a genotic stage. Indeed, if instead the evolutionary stage of the ancestors of bacteria and archaea had been the cellular one, then observing the origin of the protein moieties of the RNase P would have been, to some extent, anomalous because this completion should have already occurred, simply because the transformation of a ribozyme into an enzyme should have already taken place precisely because it falls within the very definition of the cellular status. The conclusion is that both the LUCA and the ancestor of archaea and that of bacteria may have been progenotes. If these arguments were true then either the tree of life as commonly understood would not exist and therefore the main phyletic lineages would have originated directly from the LUCA, or there would have been at least two different populations of progenotes that would have finally defined the domain of bacteria and that of archaea.

Errors of the ancestral translation, LUCA, and nature of its direct descendants

I analyzed the implications of the observation that the methyltransferases, Trm5 and TrmD, which perform the methylation of the 37th base (m1G37) in tRNAs of bacteria and archaea respectively, are not homologous proteins. The first implication is that these methyltransferases originated very late only when the fundamental lineages leading to bacteria and archaea had separated, otherwise the two methyltransferases would have been homologous enzymes, which they are not. The conclusion that Trm5 and TrmD originated only when the main lineages were defined would imply that at least some aspects of the translation, such as +1 frameshifting, were still in rapid and progressive evolution, that is, they were still originating. This would in itself imply a high rate of translation errors because the absence of m1G37 from tRNAs could have determined a high rate of +1 translational frameshifting in the reading of mRNAs, identifying this stage as that of a phase of the origin of the genetic code. Furthermore, the observation that the frameshifting mechanism was still in rapid and progressive evolution in such an advanced evolutionary stage would imply that other mechanisms concerning translation were still rapidly evolving simply because it would be very unique if only the frameshifting mechanism were the only one still originating. Importantly, the observation that in archaea m1G37 also acts as a determinant of the identity of the tRNACysGCA would imply in itself that some aspects of the origin of the genetic code were still originating, greatly strengthening the hypothesis that other aspects of the translation apparatus were still in rapid and progressive evolution. Then, all this would imply a status of progenote for LUCA and ancestors of archaea and bacteria because a high rate of translation errors would fall within the definition of progenote.

LUCA as well as the ancestors of archaea, bacteria and eukaryotes were progenotes: Inference from the distribution and diversity of the reading mechanism of the AUA and AUG codons in the domains of life

Here I use the rationale assuming that if of a certain trait that exerts its function in some aspect of the genetic code or, more generally, in protein synthesis, it is possible to identify the evolutionary stage of its origin then it would imply that this evolutionary moment would be characterized by a high translational noise because this trait would originate for the first time during that evolutionary stage. That is to say, if this trait had a non-marginal role in the realization of the genetic code, or in protein synthesis, then the origin of this trait would imply that, more generally, it was the genetic code itself that was still originating. But if the genetic code were still originating - at that precise evolutionary stage - then this would imply that there was a high translational noise which in turn would imply that it was in the presence of a protocell, i.e. a progenote that was by definition characterized by high translational noise. I apply this rationale to the mechanism of modification of the base 34 of the anticodon of an isoleucine tRNA that leads to the reading of AUA and AUG codons in archaea, bacteria and eukaryotes. The phylogenetic distribution of this mechanism in these phyletic lineages indicates that this mechanism originated only after the evolutionary stage of the last universal common ancestor (LUCA), namely, during the formation of cellular domains, i.e., at the stage of ancestors of these main phyletic lineages. Furthermore, given that this mechanism of modification of the base 34 of the anticodon of the isoleucine tRNA would result to emerge at a stage of the origin of the genetic code - despite in its terminal phases - then all this would imply that the ancestors of bacteria, archaea and eukaryotes were progenotes. If so, all the more so, the LUCA would also be a progenote since it preceded these ancestors temporally. A consequence of all this reasoning might be that since these three ancestors were of the progenotes that were different from each other, if at least one of them had evolved into at least two real and different cells - basically different from each other - then the number of cellular domains would not be three but it would be greater than three.

The phylogenetic distribution of the glutaminyl-tRNA synthetase and Glu-tRNAGln amidotransferase in the fundamental lineages would imply that the ancestor of archaea, that of eukaryotes and LUCA were progenotes

The function of the glutaminyl-tRNA synthetase and Glu-tRNAGln amidotransferase might be related to the origin of the genetic code because, for example, glutaminyl-tRNA synthetase catalyses the fundamental reaction that makes the genetic code. If the evolutionary stage of the origin of these two enzymes could be unambiguously identified, then the genetic code should still have been originating at that particular evolutionary stage because the fundamental reaction that makes the code itself was still evidently evolving. This would result in that particular evolutionary moment being attributed to the evolutionary stage of the progenote because it would have a relationship between the genotype and the phenotype not yet fully realized because the genetic code was precisely still originating. I then analyzed the distribution of the glutaminyl-tRNA synthetase and Glu-tRNAGln aminodotrasferase in the main phyletic lineages. Since in some cases the origin of these two enzymes can be related to the evolutionary stages of ancestors of archaea and eukaryotes, this would indicate these ancestors as progenotes because at that evolutionary moment the genetic code was evidently still evolving, thus realizing the definition of progenote. The conclusion that the ancestor of archaea and that of eukaryotes were progenotes would imply that even the last universal common ancestor (LUCA) was a progenote because it appeared, on the tree of life, temporally before these ancestors.

Genome-Wide Analysis Reveals Ancestral Lack of Seventeen Different tRNAs and Clade-Specific Loss of tRNA-CNNs in Archaea.

Transfer RNA (tRNA) is a category of RNAs that specifically decode messenger RNAs (mRNAs) into proteins by recognizing a set of 61 codons commonly adopted by different life domains. The composition and abundance of tRNAs play critical roles in shaping codon usage and pairing bias, which subsequently modulate mRNA translation efficiency and accuracy. Over the past few decades, effort has been concentrated on evaluating the specificity and redundancy of different tRNA families. However, the mechanism and processes underlying tRNA evolution have only rarely been investigated. In this study, by surveying tRNA genes in 167 completely sequenced genomes, we systematically investigated the composition and evolution of tRNAs in Archaea from a phylogenetic perspective. Our data revealed that archaeal genomes are compact in both tRNA types and copy number. Generally, no more than 44 different types of tRNA are present in archaeal genomes to decode the 61 canonical codons, and most of them have only one gene copy per genome. Among them, tRNA-Met was significantly overrepresented, with an average of three copies per genome. In contrast, the tRNA-UAU and 16 tRNAs with A-starting anticodons (tRNA-ANNs) were rarely detected in all archaeal genomes. The conspicuous absence of these tRNAs across the archaeal phylogeny suggests they might have not been evolved in the common ancestor of Archaea, rather than have lost independently from different clades. Furthermore, widespread absence of tRNA-CNNs in the Methanococcales and Methanobacteriales genomes indicates convergent loss of these tRNAs in the two clades. This clade-specific tRNA loss may be attributing to the reductive evolution of their genomes. Our data suggest that the current tRNA profiles in Archaea are contributed not only by the ancestral tRNA composition, but also by differential maintenance and loss of redundant tRNAs.

On Earth, there would be a number of fundamental kinds of primary cells – cellular domains – greater than or equal to four

In the studies regarding the deep nodes of the tree of life, there is an assumption that might be false. Usually, it is assumed that these nodes – that is to say, those for example regarding the ancestors of bacteria and archaea – are believed to be completely evolved cells and not protocells. In other words, in these studies, it is rarely stressed that, on the contrary, these nodes might correspond to evolutionary stages of premature cells, namely, progenotes. This observation has extremely relevant consequences. Indeed, if the nodes, for example, of the ancestors of bacteria and archaea would correspond to progenotic evolutionary stages, then this should imply that the number of fundamental kinds of primary cells (cellular domains), present on Earth, would be at least four and not two or three as it is currently believed. As a matter of fact, if these two nodes would correspond to two progenotes then, evidently, the fully evolved cells (genotes) – to which we should refer to be able to establish how many fundamental kinds of primary cells are present on Earth – would characterize less deep nodes of these two. Thus, since there is a strong evidence that the ancestors of archaea and bacteria have been of progenotes, these reasonings would assume a particular importance. For instance, it is maintained that one of these fundamental primary cells might be represented by the typical cell of superphylum of the DPANN. In other words, the DPANN superphylum might be a so far non-recognized cellular domain of life.

Phylogenetic analysis of housekeeping Archaeal proteins and early stages of Archaea evolution

The most probable horizontal gene transfer events in the evolution of Archaea are reconstructed based on the comparison of phylogenetic trees of housekeeping orthologous protein families with consensus phylogenies of Archaea. The existence of these phenomena suggests that the common ancestor of Archaea was of methanogenic and hyperthermophilic nature and dwelt in communities with a high level of ecological integration.

The common ancestor of archaea and eukarya was not an archaeon.

It is often assumed that eukarya originated from archaea. This view has been recently supported by phylogenetic analyses in which eukarya are nested within archaea. Here, I argue that these analyses are not reliable, and I critically discuss archaeal ancestor scenarios, as well as fusion scenarios for the origin of eukaryotes. Based on recognized evolutionary trends toward reduction in archaea and toward complexity in eukarya, I suggest that their last common ancestor was more complex than modern archaea but simpler than modern eukaryotes (the bug in-between scenario). I propose that the ancestors of archaea (and bacteria) escaped protoeukaryotic predators by invading high temperature biotopes, triggering their reductive evolution toward the “prokaryotic” phenotype (the thermoreduction hypothesis). Intriguingly, whereas archaea and eukarya share many basic features at the molecular level, the archaeal mobilome resembles more the bacterial than the eukaryotic one. I suggest that selection of different parts of the ancestral virosphere at the onset of the three domains played a critical role in shaping their respective biology. Eukarya probably evolved toward complexity with the help of retroviruses and large DNA viruses, whereas similar selection pressure (thermoreduction) could explain why the archaeal and bacterial mobilomes somehow resemble each other.

Diversity and evolution of multiple orc/cdc6-adjacent replication origins in haloarchaea

BackgroundWhile multiple replication origins have been observed in archaea, considerably less is known about their evolutionary processes. Here, we performed a comparative analysis of the predicted (proved in part) orc/cdc6-associated replication origins in 15 completely sequenced haloarchaeal genomes to investigate the diversity and evolution of replication origins in halophilic Archaea.ResultsMultiple orc/cdc6-associated replication origins were predicted in all of the analyzed haloarchaeal genomes following the identification of putative ORBs (origin recognition boxes) that are associated with orc/cdc6 genes. Five of these predicted replication origins in Haloarcula hispanica were experimentally confirmed via autonomous replication activities. Strikingly, several predicted replication origins in H. hispanica and Haloarcula marismortui are located in the distinct regions of their highly homologous chromosomes, suggesting that these replication origins might have been introduced as parts of new genomic content. A comparison of the origin-associated Orc/Cdc6 homologs and the corresponding predicted ORB elements revealed that the replication origins in a given haloarchaeon are quite diverse, while different haloarchaea can share a few conserved origins. Phylogenetic and genomic context analyses suggested that there is an original replication origin (oriC1) that was inherited from the ancestor of archaea, and several other origins were likely evolved and/or translocated within the haloarchaeal species.ConclusionThis study provides detailed information about the diversity of multiple orc/cdc6-associated replication origins in haloarchaeal genomes, and provides novel insight into the evolution of multiple replication origins in Archaea.

Early Evolution of Membrane Lipids: How did the Lipid Divide Occur?

The ubiquitous distribution, homology over three domains, and key role in the membrane formation of the enzymes of the CDP-alcohol phosphatidyltransferase family, as well as phylogenetic analyses of lipid synthesizing enzymes suggest that the membranes of Wächtershäuser's hypothetical pre-cells (universal common ancestor) [Mol Microbiol 47:13-22 (2003)] comprised a lipid bilayer with four types of core lipids [G-1-P-isoprenoid ether (Ai), G-3-P-fatty acyl ester (Bf), G-1-P-fatty acyl ester (Af) and G-3-P-isoprenoid ether (Bi)]. Here, a complementary hypothesis is presented to explain the difference between archaeal and bacterial lipids (lipid divide). The main driving force of lipid segregation is assumed to be glycerophosphate (GP) enantiomers, as Wächtershäuser proposed, but in the present study the hydrocarbon chains bound to each backbone are also hypothesized to affect lipid segregation. It is assumed that segregation was stimulated by different hydrocarbon chains bound to different GP backbones (Ai:Bf or Af:Bi). Because Ai and Bi are diastereomers and Af and Bf are enantiomers, Ai:Bf and Af:Bi are not equivalent. G-1-P-isoprenoid ether is provisionally assumed to segregate more easily from Bf than Bi does from Af. G-1-P-isoprenoid ether and Bf could more easily achieve the more stable homochiral membranes that are the ancestors of Archaea and Bacteria. This can explain why the extant archaeal and bacterial membrane lipids are mainly composed by Ai and Bf lipids, respectively. Because polar head groups were localized in the cytoplasmic compartment of pre-cells, they were equally carried over to Archaea and Bacteria during differentiation. Consequently, the both descendants shared the main head groups of membrane phospholipids.

The Last Universal Common Ancestor (LUCA) and the Ancestors of Archaea and Bacteria were Progenotes

The tRNA split genes of Nanoarchaeum equitans and the Met-tRNA(fMet)→fMet-tRNA(fMet) pathway, identifiable as ancestral traits, and the late appearance of DNA are used to understand the evolutionary stage at which the progenote→genote transition took place. The arguments are such as to impose that not only was the last universal common ancestor (LUCA) a progenote, but the ancestors of Archaea and Bacteria were too. Therefore, the progenote→genote transition took place in a very advanced stage of the evolution of the tree of life, and only when the ancestors of Archaea and Bacteria were already defined. These conclusions are in disagreement with commonly held beliefs.

Radical views of the Tree of Life

The tripartite division of cellular organisms into three domains – the Bacteria, the Archaea and the Eukarya – has become so ingrained that most of us have all but forgotten (or did not even know) that the ancestry and relationships among these ancient lineages are far from settled. The most widely accepted view, which emerged primarily from analyses of anciently duplicated genes (Gogarten et al., 1989; Iwabe et al., 1989), places Bacteria as the basal lineage and distinct from the common ancestor of archaea and eukaryotes. Accordingly, these studies frame the Archaea, despite their appellation, as archaic but not primordial, and the three domains are each viewed as separate lineages, with archaea and eukaryotes as sister taxa. Early on, Lake (1988) developed an algorithm that positioned a clade of thermophilic, sulfur-metabolizing archaea (the Crenarchaeaota or ‘eocytes’) as more closely related to eukaryotes than to other archaea, and the archael Holobacteria as more closely related to Eubacteria. This upended the view that Bacteria, Archaea and Eukarya were separate divisions; however, subsequent analyses of small- and large-subunit rRNA sequences in more conventional phylogenetic frameworks upheld the Archaea as a cohesive group (Gouy

Evaluating hypotheses for the origin of eukaryotes

Numerous scenarios explain the origin of the eukaryote cell by fusion or endosymbiosis between an archaeon and a bacterium (and sometimes a third partner). We evaluate these hypotheses using the following three criteria. Can the data be explained by the null hypothesis that new features arise sequentially along a stem lineage? Second, hypotheses involving an archaeon and a bacterium should undergo standard phylogenetic tests of gene distribution. Third, accounting for past events by processes observed in modern cells is preferable to postulating unknown processes that have never been observed. For example, there are many eukaryote examples of bacteria as endosymbionts or endoparasites, but none known in archaea. Strictly post-hoc hypotheses that ignore this third criterion should be avoided. Applying these three criteria significantly narrows the number of plausible hypotheses. Given current knowledge, our conclusion is that the eukaryote lineage must have diverged from an ancestor of archaea well prior to the origin of the mitochondrion. Significantly, the absence of ancestrally amitochondriate eukaryotes (archezoa) among extant eukaryotes is neither evidence for an archaeal host for the ancestor of mitochondria, nor evidence against a eukaryotic host.

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.

Looking for the most “primitive” organism(s) on Earth today: the state of the art

Molecular phylogenetic studies have revealed a tripartite division of the living world into two procaryotic groups, Bacteria and Archaea, and one eucaryotic group, Eucarya. Which group is the most “primitive”? Which groups are sister? The answer to these questions would help to delineate the characters of the last common ancestor to all living beings, as a first step to reconstruct the earliest periods of biological evolution on Earth. The current “Procaryotic dogma” claims that procaryotes are primitive. Since the ancestor of Archaea was most probably a hyperthermophile, and since bacteria too might have originated from hyperthermophiles, the procaryotic dogma has been recently connected to the hot origin of life hypothesis. However, the notion that present-day hyperthermophiles are primitive has been challenged by recent findings, in these unique microorganisms, of very elaborate adaptative devices for life at high temperature. Accordingly, I discuss here alternative hypotheses that challenge the procaryotic dogma, such as the idea of a universal ancestor with molecular features in between those of eucaryotes and procaryotes, or the origin of procaryotes via thermophilic adaptation. Clearly, major evolutionary questions about early cellular evolution on Earth remain to be settled before we can speculate with confidence about which kinds of life might have appeared on other planets.