On the Origin of Cells and Viruses: A Comparative-Genomic Perspective

2006 ◽  
Vol 52 (3-4) ◽  
pp. 299-318 ◽  
Author(s):  
Eugene V. Koonin
Keyword(s):  
Biological Evolution ◽  
Empirical Support ◽  
Molecular Complexes ◽  
Life Forms ◽  
Comparative Genomic ◽  
Cellular Origin ◽  
Cellular Life ◽  
Universal Common Ancestor ◽  
Replication Systems ◽  
Lines Of Descent

It is proposed that the pre-cellular stage of biological evolution, including the Last Universal Common Ancestor (LUCA) of modern cellular life forms, occurred within networks of inorganic compartments that hosted a diverse mix of virus-like genetic elements. This viral model of cellular origin recapitulates the early ideas of J.B.S. Haldane, sketched in his 1928 essay on the origin of life. However, unlike in Haldane's day, there is substantial empirical support for this scenario from three major lines of evidence provided by comparative genomics: (i) the lack of homology among the core components of the DNA replication systems between the two primary lines of descent of cellular life forms, archaea and bacteria, (ii) the similar lack of homology between the enzymes of lipid biosynthesis in conjunction with distinct membrane chemistries in archaea and bacteria, and (iii) the spread of several viral hallmark genes, which encode proteins with key functions in viral replication and morphogenesis, among numerous and extremely diverse groups of viruses, in contrast to their absence in cellular life forms. Under the viral model of pre-cellular evolution, the key elements of cells including the replication apparatus, membranes, molecular complexes involved in membrane transport and translocation, and others originated as components of virus-like entities. This model alleviates, at least in part, the challenge of the emergence of the immensely complex organization of modern cells.

scholarly journals Viruses and mobile elements as drivers of evolutionary transitions

2016 ◽  
Vol 371 (1701) ◽  
pp. 20150442 ◽  
Author(s):  
Eugene V. Koonin
Keyword(s):  
Genomic Analysis ◽  
Life Forms ◽  
Comparative Genomic ◽  
Biological Organization ◽  
Evolutionary Transitions ◽  
Selfish Genetic Elements ◽  
Cellular Life ◽  
History Of ◽  
Eusocial Animals ◽  
Multicellular Organisms

The history of life is punctuated by evolutionary transitions which engender emergence of new levels of biological organization that involves selection acting at increasingly complex ensembles of biological entities. Major evolutionary transitions include the origin of prokaryotic and then eukaryotic cells, multicellular organisms and eusocial animals. All or nearly all cellular life forms are hosts to diverse selfish genetic elements with various levels of autonomy including plasmids, transposons and viruses. I present evidence that, at least up to and including the origin of multicellularity, evolutionary transitions are driven by the coevolution of hosts with these genetic parasites along with sharing of ‘public goods’. Selfish elements drive evolutionary transitions at two distinct levels. First, mathematical modelling of evolutionary processes, such as evolution of primitive replicator populations or unicellular organisms, indicates that only increasing organizational complexity, e.g. emergence of multicellular aggregates, can prevent the collapse of the host–parasite system under the pressure of parasites. Second, comparative genomic analysis reveals numerous cases of recruitment of genes with essential functions in cellular life forms, including those that enable evolutionary transitions. This article is part of the themed issue ‘The major synthetic evolutionary transitions’.

scholarly journals Jumbo Phages: A Comparative Genomic Overview of Core Functions and Adaptions for Biological Conflicts

Viruses ◽  
2021 ◽  
Vol 13 (1) ◽  
pp. 63
Author(s):  
Lakshminarayan M. Iyer ◽  
Vivek Anantharaman ◽  
Arunkumar Krishnan ◽  
A. Maxwell Burroughs ◽  
L. Aravind
Keyword(s):  
Genome Size ◽  
Principal Component ◽  
Comparative Genomic ◽  
Rna Repair ◽  
Cellular Life ◽  
Rna Targeting ◽  
Conserved Genes ◽  
Comparative Genomics Analysis ◽  
Phage Proteins ◽  
Novel Protein

Jumbo phages have attracted much attention by virtue of their extraordinary genome size and unusual aspects of biology. By performing a comparative genomics analysis of 224 jumbo phages, we suggest an objective inclusion criterion based on genome size distributions and present a synthetic overview of their manifold adaptations across major biological systems. By means of clustering and principal component analysis of the phyletic patterns of conserved genes, all known jumbo phages can be classified into three higher-order groups, which include both myoviral and siphoviral morphologies indicating multiple independent origins from smaller predecessors. Our study uncovers several under-appreciated or unreported aspects of the DNA replication, recombination, transcription and virion maturation systems. Leveraging sensitive sequence analysis methods, we identify novel protein-modifying enzymes that might help hijack the host-machinery. Focusing on host–virus conflicts, we detect strategies used to counter different wings of the bacterial immune system, such as cyclic nucleotide- and NAD+-dependent effector-activation, and prevention of superinfection during pseudolysogeny. We reconstruct the RNA-repair systems of jumbo phages that counter the consequences of RNA-targeting host effectors. These findings also suggest that several jumbo phage proteins provide a snapshot of the systems found in ancient replicons preceding the last universal ancestor of cellular life.

scholarly journals Inseparable tandem: evolution chooses ATP and Ca 2+ to control life, death and cellular signalling

2016 ◽  
Vol 371 (1700) ◽  
pp. 20150419 ◽  
Author(s):  
Helmut Plattner ◽  
Alexei Verkhratsky
Keyword(s):  
Intracellular Transport ◽  
Extended Family ◽  
Calcium Phosphates ◽  
Atmospheric Oxygen ◽  
Biological Evolution ◽  
Life Forms ◽  
Amoeboid Movement ◽  
Atp Production ◽  
Flagellar Beat ◽  
Signalling Molecule

From the very dawn of biological evolution, ATP was selected as a multipurpose energy-storing molecule. Metabolism of ATP required intracellular free Ca 2+ to be set at exceedingly low concentrations, which in turn provided the background for the role of Ca 2+ as a universal signalling molecule. The early-eukaryote life forms also evolved functional compartmentalization and vesicle trafficking, which used Ca 2+ as a universal signalling ion; similarly, Ca 2+ is needed for regulation of ciliary and flagellar beat, amoeboid movement, intracellular transport, as well as of numerous metabolic processes. Thus, during evolution, exploitation of atmospheric oxygen and increasingly efficient ATP production via oxidative phosphorylation by bacterial endosymbionts were a first step for the emergence of complex eukaryotic cells. Simultaneously, Ca 2+ started to be exploited for short-range signalling, despite restrictions by the preset phosphate-based energy metabolism, when both phosphates and Ca 2+ interfere with each other because of the low solubility of calcium phosphates. The need to keep cytosolic Ca 2+ low forced cells to restrict Ca 2+ signals in space and time and to develop energetically favourable Ca 2+ signalling and Ca 2+ microdomains. These steps in tandem dominated further evolution. The ATP molecule (often released by Ca 2+ -regulated exocytosis) rapidly grew to be the universal chemical messenger for intercellular communication; ATP effects are mediated by an extended family of purinoceptors often linked to Ca 2+ signalling. Similar to atmospheric oxygen, Ca 2+ must have been reverted from a deleterious agent to a most useful (intra- and extracellular) signalling molecule. Invention of intracellular trafficking further increased the role for Ca 2+ homeostasis that became critical for regulation of cell survival and cell death. Several mutually interdependent effects of Ca 2+ and ATP have been exploited in evolution, thus turning an originally unholy alliance into a fascinating success story. This article is part of the themed issue ‘Evolution brings Ca 2+ and ATP together to control life and death’.

scholarly journals Multiple evolutionary origins of giant viruses

F1000Research ◽  
2018 ◽  
Vol 7 ◽  
pp. 1840 ◽  
Author(s):  
Eugene V. Koonin ◽  
Natalya Yutin
Keyword(s):  
Life Forms ◽  
Translation System ◽  
Dna Viruses ◽  
Evolutionary Forces ◽  
Evolutionary Origins ◽  
Cellular Life ◽  
Giant Viruses ◽  
Nucleocytoplasmic Large Dna Viruses ◽  
Phylogenomic Analyses ◽  
Definition Of

The nucleocytoplasmic large DNA viruses (NCLDVs) are a monophyletic group of diverse eukaryotic viruses that reproduce primarily in the cytoplasm of the infected cells and include the largest viruses currently known: the giant mimiviruses, pandoraviruses, and pithoviruses. With virions measuring up to 1.5 μm and genomes of up to 2.5 Mb, the giant viruses break the now-outdated definition of a virus and extend deep into the genome size range typical of bacteria and archaea. Additionally, giant viruses encode multiple proteins that are universal among cellular life forms, particularly components of the translation system, the signature cellular molecular machinery. These findings triggered hypotheses on the origin of giant viruses from cells, likely of an extinct fourth domain of cellular life, via reductive evolution. However, phylogenomic analyses reveal a different picture, namely multiple origins of giant viruses from smaller NCLDVs via acquisition of multiple genes from the eukaryotic hosts and bacteria, along with gene duplication. Thus, with regard to their origin, the giant viruses do not appear to qualitatively differ from the rest of the virosphere. However, the evolutionary forces that led to the emergence of virus gigantism remain enigmatic.

The regulatory roles and mechanism of transcriptional pausing

2006 ◽  
Vol 34 (6) ◽  
pp. 1062-1066 ◽  
Author(s):  
R. Landick
Keyword(s):  
Single Molecule ◽  
Life Forms ◽  
Eukaryotic Transcription ◽  
Regulatory Interactions ◽  
Enzymatic Mechanism ◽  
Cellular Life ◽  
Efficient Gene ◽  
Transcriptional Pausing ◽  
Elongation Phase ◽  
Fundamental Mechanism

The multisubunit RNAPs (RNA polymerases) found in all cellular life forms are remarkably conserved in fundamental structure, in mechanism and in their susceptibility to sequence-dependent pausing during transcription of DNA in the absence of elongation regulators. Recent studies of both prokaryotic and eukaryotic transcription have yielded an increasing appreciation of the extent to which gene regulation is accomplished during the elongation phase of transcription. Transcriptional pausing is a fundamental enzymatic mechanism that underlies many of these regulatory schemes. In some cases, pausing functions by halting RNAP for times or at positions required for regulatory interactions. In other cases, pauses function by making RNAP susceptible to premature termination of transcription unless the enzyme is modified by elongation regulators that programme efficient gene expression. Pausing appears to occur by a two-tiered mechanism in which an initial rearrangement of the enzyme's active site interrupts active elongation and puts RNAP in an elemental pause state from which additional rearrangements or regulator interactions can create long-lived pauses. Recent findings from biochemical and single-molecule transcription experiments, coupled with the invaluable availability of RNAP crystal structures, have produced attractive hypotheses to explain the fundamental mechanism of pausing.

scholarly journals Origin of life: LUCA and extracellular membrane vesicles (EMVs)

2015 ◽  
Vol 15 (1) ◽  
pp. 7-15 ◽  
Author(s):  
S. Gill ◽  
P. Forterre
Keyword(s):  
Common Ancestor ◽  
Membrane Vesicles ◽  
Last Universal Common Ancestor ◽  
Molecular Systems ◽  
Cellular Physiology ◽  
Cellular Life ◽  
Universal Common Ancestor ◽  
Domains Of Life ◽  
Metabolic Reactions

AbstractCells from the three domains of life produce extracellular membrane vesicles (EMVs), suggesting that EMV production is an important aspect of cellular physiology. EMVs have been implicated in many aspects of cellular life in all domains, including stress response, toxicity against competing strains, pathogenicity, detoxification and resistance against viral attack. These EMVs represent an important mode of inter-cellular communication by serving as vehicles for transfer of DNA, RNA, proteins and lipids between cells. Here, we review recent progress in the understanding of EMV biology and their various roles. We focus on the role of membrane vesicles in early cellular evolution and how they would have helped shape the nature of the last universal common ancestor. A membrane-protected micro-environment would have been a key to the survival of spontaneous molecular systems and efficient metabolic reactions. Interestingly, the morphology of EMVs is strongly reminiscent of the morphology of some virions. It is thus tempting to make a link between the origin of the first protocell via the formation of vesicles and the origin of viruses.

scholarly journals The Compressed Vocabulary of Microbial Life

2021 ◽  
Vol 12 ◽  
Author(s):  
Gustavo Caetano-Anollés
Keyword(s):  
Evolutionary Strategies ◽  
Module Structure ◽  
Microbial World ◽  
Scale Free ◽  
Microbial Life ◽  
Size Dependent ◽  
Cellular Life ◽  
Universal Common Ancestor ◽  
Evolutionary Genomic ◽  
The Impact

Communication is an undisputed central activity of life that requires an evolving molecular language. It conveys meaning through messages and vocabularies. Here, I explore the existence of a growing vocabulary in the molecules and molecular functions of the microbial world. There are clear correspondences between the lexicon, syntax, semantics, and pragmatics of language organization and the module, structure, function, and fitness paradigms of molecular biology. These correspondences are constrained by universal laws and engineering principles. Macromolecular structure, for example, follows quantitative linguistic patterns arising from statistical laws that are likely universal, including the Zipf’s law, a special case of the scale-free distribution, the Heaps’ law describing sublinear growth typical of economies of scales, and the Menzerath–Altmann’s law, which imposes size-dependent patterns of decreasing returns. Trade-off solutions between principles of economy, flexibility, and robustness define a “triangle of persistence” describing the impact of the environment on a biological system. The pragmatic landscape of the triangle interfaces with the syntax and semantics of molecular languages, which together with comparative and evolutionary genomic data can explain global patterns of diversification of cellular life. The vocabularies of proteins (proteomes) and functions (functionomes) revealed a significant universal lexical core supporting a universal common ancestor, an ancestral evolutionary link between Bacteria and Eukarya, and distinct reductive evolutionary strategies of language compression in Archaea and Bacteria. A “causal” word cloud strategy inspired by the dependency grammar paradigm used in catenae unfolded the evolution of lexical units associated with Gene Ontology terms at different levels of ontological abstraction. While Archaea holds the smallest, oldest, and most homogeneous vocabulary of all superkingdoms, Bacteria heterogeneously apportions a more complex vocabulary, and Eukarya pushes functional innovation through mechanisms of flexibility and robustness.

scholarly journals Stability of host-parasite systems: you must differ to coevolve

2018 ◽  
Author(s):  
Faina Berezovskaya ◽  
Georgy P. Karev ◽  
Mikhail I. Katsnelson ◽  
Yuri I. Wolf ◽  
Eugene V. Koonin
Keyword(s):  
Bifurcation Analysis ◽  
Carrying Capacity ◽  
Life Forms ◽  
Entire System ◽  
Modified Model ◽  
Cellular Life ◽  
Trivial Equilibrium ◽  
The Stability ◽  
Host Parasite ◽  
Theoretical Considerations

AbstractBackgroundGenetic parasites are ubiquitous satellites of cellular life forms most of which host a variety of mobile genetic elements including transposons, plasmids and viruses. Theoretical considerations and computer simulations suggest that emergence of genetic parasites is intrinsic to evolving replicator systems.ResultsUsing methods of bifurcation analysis, we investigated the stability of simple models of replicator-parasite coevolution in a well-mixed environment. It is shown that the simplest imaginable system of this type, one in which the parasite evolves during the replication of the host genome through a minimal mutation that renders the genome of the emerging parasite incapable of producing the replicase but able to recognize and recruit it for its own replication, is unstable. In this model, there are only either trivial or “semi-trivial”, parasite-free equilibria: an inefficient parasite is outcompeted by the host and dies off whereas an efficient one pushes the host out of existence, which leads to the collapse of the entire system. We show that stable host-parasite coevolution (a non-trivial equilibrium) is possible in a modified model where the parasite is qualitatively distinct from the host replicator in that the replication of the parasite depends solely on the availability of the host but not on the carrying capacity of the environment.ConclusionsWe analytically determine the conditions for stable host-parasite coevolution in simple mathematical models and find that a parasite that initially evolves from the host through the loss of the ability to replicate autonomously must be substantially derived for a stable host-parasite coevolution regime to be established.

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