Vesiduction: the fourth way of HGT Soler, Nicolas; Forterre, Patrick
Environmental microbiology,
July 2020, Letnik:
22, Številka:
7
Journal Article
Recenzirano
Summary
Besides the canonical gene transfer mechanisms transformation, transduction and conjugation, DNA transfer involving extracellular vesicles is still under appreciated. However, this widespread ...phenomenon has been observed in the three domains of life. Here, we propose the term ‘Vesiduction’ as a fourth mode of intercellular DNA transfer.
Recently, several authors have suggested that viruses are ancient organisms that should be introduced in evolutionary scenarios describing the history of life. However, these views have been strongly ...disputed by authors who support the traditional view of viruses as byproducts of cellular activity. For a long time, viruses have been indeed confused with virions, inert particles without metabolic activity, excluding them from the realm of life. I introduce here the concept of virocell, to put emphasis on the intracellular phase of the virus life cycle. This concept posits that viruses are cellular – thus living – organisms, and highlight the capacity of viruses to create new genes to manipulate their cellular environment and to create novel biological mechanisms. This concept helps to explain why viruses have played a major role in the history of life. It suggests to mine more systematically the viral world to find new tools for synthetic biology.
Récemment, plusieurs auteurs ont souligné l’ancienneté des virus et la nécessité de les prendre en compte dans les scénarios évolutifs. Ces idées sont toutefois contestées par les tenants de la vision traditionnelle selon laquelle les virus sont essentiellement des sous-produits de l’activité cellulaire. En effet, pendant longtemps, les virus ont été confondus avec les virions, des particules inertes sans activité métabolique. Ils ne répondaient donc pas à la définition classique des êtres vivants. Je propose ici la notion de cellule virale (
virocell) qui met en avant la phase intracellulaire du cycle viral. Ce concept considère les virus comme des organismes cellulaires, donc vivant, met en avant leur capacité à créer de nouveaux gènes et de nouveaux mécanismes biologiques. Cette capacité explique pourquoi les virus ont joué un rôle si important dans l’histoire du vivant. Les virus sont donc passés maîtres en biologie synthétique, et leur exemple pourrait nous inspirer.
The curiosity-driven discovery of giant DNA viruses infecting amoebas has triggered an intense debate about the origin, nature, and definition of viruses. This discovery was delayed by the current ...paradigm confusing viruses with small virions. Several new definitions and concepts have been proposed either to reconcile the unique features of giant viruses with previous paradigms or to propose a completely new vision of the living world. I briefly review here how several other lines of research in virology converged during the last 2 decades with the discovery of giant viruses to change our traditional perception of the viral world. This story emphasizes the power of multidisciplinary curiosity-driven research, from the hospital to the field and the laboratory. Notably, some philosophers have now also joined biologists in their quest to make sense of the abundance and diversity of viruses and related capsidless mobile elements in the biosphere.
Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the ...eukaryotic virome. However, their origin(s), evolution, and potential roles in the emergence of modern eukaryotes remain subjects of intense debate. Here we present robust phylogenetic trees of NCLDVs, based on the 8 most conserved proteins responsible for virion morphogenesis and informational processes. Our results uncover the evolutionary relationships between different NCLDV families and support the existence of 2 superclades of NCLDVs, each encompassing several families. We present evidence strongly suggesting that the NCLDV core genes, which are involved in both informational processes and virion formation, were acquired vertically from a common ancestor. Among them, the largest subunits of the DNA-dependent RNA polymerase were transferred between 2 clades of NCLDVs and proto-eukaryotes, giving rise to 2 of the 3 eukaryotic DNA-dependent RNA polymerases. Our results strongly suggest that these transfers and the diversification of NCLDVs predated the emergence of modern eukaryotes, emphasizing the major role of viruses in the evolution of cellular domains.
Our conceptions on the origin, nature, and role of viruses have been shaken recently by several independent lines of research. There are many reasons to believe now that viruses are more ancient than ...modern cells and have always been more abundant and diverse than their cellular targets. Viruses can be defined as capsid‐encoding organisms that transform their “host” cell into a viral factory. If capsid‐encoding organisms (viruses) and ribosome‐encoding organisms (cells) are the major types of living entities on our planet, it seems logical to conclude that their conflict has been a major engine of biological evolution (in the framework of natural selection). In particular, many novelties first selected in the viral world might have been transferred to cells as a consequence of the continuous flow of viral genes into cellular genomes. We discuss recent observations and hypotheses suggesting that viruses have played a major role at different stages of biological evolution, such as the RNA to DNA transition, the origin of the eukaryotic nucleus, or, alternatively, the origin of unique features in multicellular macrobes.
Comment on: Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature. 2015 Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and ...eukaryotes. PLoS Genet. 2017
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
The eocyte hypothesis, in which Eukarya emerged from within Archaea, has been boosted by the description of a new candidate archaeal phylum, "Lokiarchaeota", from metagenomic data. Eukarya branch ...within Lokiarchaeota in a tree reconstructed from the concatenation of 36 universal proteins. However, individual phylogenies revealed that lokiarchaeal proteins sequences have different evolutionary histories. The individual markers phylogenies revealed at least two subsets of proteins, either supporting the Woese or the Eocyte tree of life. Strikingly, removal of a single protein, the elongation factor EF2, is sufficient to break the Eukaryotes-Lokiarchaea affiliation. Our analysis suggests that the three lokiarchaeal EF2 proteins have a chimeric organization that could be due to contamination and/or homologous recombination with patches of eukaryotic sequences. A robust phylogenetic analysis of RNA polymerases with a new dataset indicates that Lokiarchaeota and related phyla of the Asgard superphylum are sister group to Euryarchaeota, not to Eukarya, and supports the monophyly of Archaea with their rooting in the branch leading to Thaumarchaeota.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
The division of the living world into three cellular domains, Archaea, Bacteria, and Eukarya, is now generally accepted. However, there is no consensus about the evolutionary relationships among ...these domains, because all of the proposed models have a number of more or less severe pitfalls. Another drawback of current models for the universal tree of life is the exclusion of viruses, otherwise a major component of the biosphere. Recently, it was suggested that the transition from RNA to DNA genomes occurred in the viral world, and that cellular DNA and its replication machineries originated via transfers from DNA viruses to RNA cells. Here, I explore the possibility that three such independent transfers were at the origin of Archaea, Bacteria, and Eukarya, respectively. The reduction of evolutionary rates following the transition from RNA to DNA genomes would have stabilized the three canonical versions of proteins involved in translation, whereas the existence of three different founder DNA viruses explains why each domain has its specific DNA replication apparatus. In that model, plasmids can be viewed as transitional forms between DNA viruses and cellular chromosomes, and the formation of different levels of cellular organization (prokaryote or eukaryote) could be traced back to the nature of the founder DNA viruses and RNA cells.
The Microviridae comprises icosahedral lytic viruses with circular single-stranded DNA genomes. The family is divided into two distinct groups based on genome characteristics and virion structure. ...Viruses infecting enterobacteria belong to the genus Microvirus, whereas those infecting obligate parasitic bacteria, such as Chlamydia, Spiroplasma and Bdellovibrio, are classified into a subfamily, the Gokushovirinae. Recent metagenomic studies suggest that members of the Microviridae might also play an important role in marine environments. In this study we present the identification and characterization of Microviridae-related prophages integrated in the genomes of species of the Bacteroidetes, a phylum not previously known to be associated with microviruses. Searches against metagenomic databases revealed the presence of highly similar sequences in the human gut. This is the first report indicating that viruses of the Microviridae lysogenize their hosts. Absence of associated integrase-coding genes and apparent recombination with dif-like sequences suggests that Bacteroidetes-associated microviruses are likely to rely on the cellular chromosome dimer resolution machinery. Phylogenetic analysis of the putative major capsid proteins places the identified proviruses into a group separate from the previously characterized microviruses and gokushoviruses, suggesting that the genetic diversity and host range of bacteriophages in the family Microviridae is wider than currently appreciated.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Abstract
Reverse gyrase (RG) is the only protein found ubiquitously in hyperthermophilic organisms, but absent from mesophiles. As such, its simple presence or absence allows us to deduce information ...about the optimal growth temperature of long-extinct organisms, even as far as the last universal common ancestor of extant life (LUCA). The growth environment and gene content of the LUCA has long been a source of debate in which RG often features. In an attempt to settle this debate, we carried out an exhaustive search for RG proteins, generating the largest RG data set to date. Comprising 376 sequences, our data set allows for phylogenetic reconstructions of RG with unprecedented size and detail. These RG phylogenies are strikingly different from those of universal proteins inferred to be present in the LUCA, even when using the same set of species. Unlike such proteins, RG does not form monophyletic archaeal and bacterial clades, suggesting RG emergence after the formation of these domains, and/or significant horizontal gene transfer. Additionally, the branch lengths separating archaeal and bacterial groups are very short, inconsistent with the tempo of evolution from the time of the LUCA. Despite this, phylogenies limited to archaeal RG resolve most archaeal phyla, suggesting predominantly vertical evolution since the time of the last archaeal ancestor. In contrast, bacterial RG indicates emergence after the last bacterial ancestor followed by significant horizontal transfer. Taken together, these results suggest a nonhyperthermophilic LUCA and bacterial ancestor, with hyperthermophily emerging early in the evolution of the archaeal and bacterial domains.
PDF
