Homologous Capsid Proteins Testify to the Common Ancestry of Retroviruses, Caulimoviruses, Pseudoviruses, and Metaviruses

Krupovìč, Mart; Koonin, Eugene V.

doi:10.1128/jvi.00210-17

Cited by 27 publications

(28 citation statements)

References 23 publications

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“…The classic case in point are reverse-transcribing elements, a class of MGE that includes both an enormous variety of non-viral elements, and bona fide viruses with an essential step of integration into the host genome in their life cycle [3,4]. Two families of viruses, Metaviridae and Pseudoviridae , primarily lead the transposon life style but retain the ability to form virions and share common ancestry with bona fide reverse-transcribing viruses [5,6]. …”

Section: Introductionmentioning

confidence: 99%

Polintons, virophages and transpovirons: a tangled web linking viruses, transposons and immunity

Koonin

Krupovìč

2017

Current Opinion in Virology

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109

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Virophages are satellite DNA viruses that depend for their replication on giant viruses of the family Mimiviridae. An evolutionary relationship exists between the virophages and Polintons, large self-synthesizing transposons that are wide spread in the genomes of diverse eukaryotes. Most of the Polintons encode homologs of major and minor icosahedral virus capsid proteins and accordingly are predicted to form virions. Additionally, metagenome analysis has led to the discovery of an expansive family of Polinton-like viruses (PLV) that are more distantly related to bona fide Polintons and virophages. Another group of giant virus parasites includes small, linear, double-stranded DNA elements called transpovirons. Recent in-depth comparative genomic analysis has yielded evidence of the origin of the PLV and the transpovirons from Polintons. Integration of virophage genomes into genomes of both giant viruses and protists has been demonstrated. Furthermore, in an experimental coinfection system that consisted of a protist host, a giant virus and an associated virophage, the virophage integrated into the host genome and, after activation of its expression by a superinfecting giant virus, served as an agent of adaptive immunity. There is a striking analogy between this mechanism and the CRISPR-Cas system of prokaryotic adaptive immunity. Taken together, these findings show that Polintons, PLV, virophages and transpovirons form a dynamic network of integrating mobile genetic elements that contribute to the cellular antivirus defense and host-virus coevolution.

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Section: Introductionmentioning

confidence: 99%

Polintons, virophages and transpovirons: a tangled web linking viruses, transposons and immunity

Koonin

Krupovìč

2017

Current Opinion in Virology

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109

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“…In contrast, hepadnaviruses encode an unrelated capsid protein (23). These findings suggest that belpaoviruses, caulimoviruses, metaviruses, pseudoviruses, and retroviruses have evolved from a common viral ancestor, rather than from distinct capsid-less retrotransposons (20).…”

mentioning

confidence: 96%

Ortervirales: New Virus Order Unifying Five Families of Reverse-Transcribing Viruses

Krupovìč

Blomberg

Coffin

et al. 2018

J Virol

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“…Given the high prevalence of the SJR and DJR CPs among viruses infecting all three domains of cellular life, these proteins most likely emerged during or shortly after the advent of modern-type bacterial and archaeal cells. By contrast, the exclusive yet ubiquitous presence of reverse-transcribing viruses in eukaryotes implies that the nucleocapsid and capsid domains of the Gag polyprotein were acquired by ancestral reverse-transcribing virus at an early stage of eukaryogenesis 109 . Furthermore, the matrix protein domain, which is specific to members of the family Retroviridae, was likely appended to the Gag polyprotein following the divergence of retroviruses from other orterviruses, probably after the emergence of vertebrates.…”

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confidence: 97%

Origin of viruses: primordial replicators recruiting capsids from hosts

2019

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Viruses are ubiquitous parasites of cellular life and the most abundant biological entities on earth. It is widely accepted that viruses are polyphyletic but a consensus scenario for their ultimate origin(s) is still lacking. Traditionally, three different scenarios have been considered for the origin of viruses: descent from primordial, pre-cellular genetic elements, reductive evolution from cellular ancestors, and escape of genes from cellular hosts achieving partial replicative autonomy and becoming parasitic genetic elements. These three classical scenarios give different timelines for the origin of viruses and do not explain the provenance of the two key functional modules that are responsible, respectively, for virus genome replication and virion morphogenesis. Here we outline a 'chimeric' scenario under which different types of primordial, selfish replicons gave rise to viruses by recruiting host proteins for virion formation. We also propose that new groups of viruses have repeatedly emerged at all stages of the evolution of life, often, through the displacement of ancestral structural and genome replication genes. [H1] Introduction Viruses are the most abundant biological entities on our planet and have major roles in global ecology and evolution of the biosphere 1-4. All cellular organisms, with the possible exception of some intracellular parasitic bacteria, harbour distinctive repertoires of viruses, that is, obligate intracellular genetic parasites that package their genomes into virus particles (virions) 5. The ubiquity of viruses, combined with the theoretical argument that genetic parasites will inevitably emerge in replicator systems 6,7 , implies that the entire course of the evolution of life is actually a story of virus-host coevolution 4,8-10. Accordingly, evolution of life cannot be understood without elucidating the origin(s) of viruses, yet, these origins currently remain mysterious. Historically, three distinct scenarios of virus origin have been considered 11-17 (Figure 1). According to the 'primordial virus world' or 'virus early' hypothesis, viruses are direct descendants of the first replicons that existed during the pre-cellular stage of the evolution of life. By contrast, in the 'reductive virus origin' or 'regression' scenario, viruses are the ultimate products of degeneration of ancestral cells that have lost their autonomy and transitioned to obligate intracellular parasitism. Finally, in the 'escaped genes' scenario, viruses evolved on multiple, independent occasions in different cellular organisms from host genes that acquired the capacity for (quasi)autonomous, selfish replication and infectivity. Accordingly, escaped bacterial, archaeal and eukaryotic genes are thought to have given rise to bacterial, 2 archaeal and eukaryotic viruses, respectively. The three scenarios seem to be mutually exclusive with respect to the origin of any particular group of viruses but different groups of viruses potentially could have evolved via different routes. Over the years, all three scenari...

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Homologous Capsid Proteins Testify to the Common Ancestry of Retroviruses, Caulimoviruses, Pseudoviruses, and Metaviruses

Cited by 27 publications

References 23 publications

Polintons, virophages and transpovirons: a tangled web linking viruses, transposons and immunity

Polintons, virophages and transpovirons: a tangled web linking viruses, transposons and immunity

Ortervirales: New Virus Order Unifying Five Families of Reverse-Transcribing Viruses

Origin of viruses: primordial replicators recruiting capsids from hosts

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