DNA Polymerase Diversity Reveals Multiple Incursions of Polintons During Nematode Evolution

Jeong, Dae-Eun; Sundrani, Sameer; Hall, Richard Nelson; Krupovic, Mart; Koonin, Eugene V; Fire, Andrew Z

doi:10.1093/molbev/msad274

Cited by 6 publications

(1 citation statement)

References 86 publications

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“…Transfer of transposable elements across closely related lineages is not uncommon ( Zhuo, Feschotte, and Belshaw 2015 ). Consistent with our observations, an analysis from a very recent study by Jeong et al. (2023 ) found the horizontal transfer of polintoviruses across different nematode strains within the same species, and even inter-phylum transfer of these elements.…”

Section: Resultssupporting

confidence: 92%

Widespread occurrence and diverse origins of polintoviruses influence lineage-specific genome dynamics in stony corals

Stephens,

Faghihi,

Moniruzzaman

2024

Virus Evolution

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Stony corals (Order Scleractinia) are central to vital marine habitats known as coral reefs. Numerous stressors in the Anthropocene are contributing to the ongoing decline in coral reef health and coverage. While viruses are established modulators of marine microbial dynamics, their interactions within the coral holobiont and impact on coral health and physiology remain unclear. To address this key knowledge gap, we investigated diverse stony coral genomes for ‘endogenous’ viruses. Our study uncovered a remarkable number of integrated viral elements recognized as ‘Polintoviruses’ (Class Polintoviricetes) in 30 Scleractinia genomes; with several species harboring hundreds to thousands of polintoviruses. We reveal massive paralogous expansion of polintoviruses in stony coral genomes, alongside presence of integrated elements closely related to Polinton-like viruses (PLVs), a group of viruses that exist as free virions. These results suggest multiple integrations of polintoviruses and PLV-relatives, along with paralogous expansions, shaped stony coral genomes. Re-analysis of existing gene expression data reveals all polintovirus structural and non-structural hallmark genes are expressed, providing support for free virion production from polintoviruses. Our results, revealing a significant diversity of polintovirus across the Scleractinia order, open a new research avenue into polintovirus and their possible roles in disease, genomic plasticity, and environmental adaptation in this key group of organisms.

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Section: Resultssupporting

confidence: 92%

Widespread occurrence and diverse origins of polintoviruses influence lineage-specific genome dynamics in stony corals

Stephens,

Faghihi,

Moniruzzaman

2024

Virus Evolution

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Natural history of eukaryotic DNA viruses with double jelly-roll major capsid proteins

Krupovic,

Kuhn,

Fischer

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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The phylum Preplasmiviricota (kingdom Bamfordvirae , realm Varidnaviria ) is a broad assemblage of diverse viruses with comparatively short double-stranded DNA genomes (<50 kbp) that produce icosahedral capsids built from double jelly-roll major capsid proteins. Preplasmiviricots infect hosts from all cellular domains, testifying to their ancient origin, and, in particular, are associated with six of the seven supergroups of eukaryotes. Preplasmiviricots comprise four major groups of viruses, namely, polintons, polinton-like viruses (PLVs), virophages, and adenovirids. We used protein structure modeling and analysis to show that protein-primed DNA polymerases (pPolBs) of polintons, virophages, and cytoplasmic linear plasmids encompass an N-terminal domain homologous to the terminal proteins (TPs) of prokaryotic PRD1-like tectivirids and eukaryotic adenovirids that are involved in protein-primed replication initiation, followed by a viral ovarian tumor–like cysteine deubiquitinylase (vOTU) domain. The vOTU domain is likely responsible for the cleavage of the TP from the large pPolB polypeptide and is inactivated in adenovirids, in which TP is a separate protein. Many PLVs and transpovirons encode a distinct derivative of polinton-like pPolB that retains the TP, vOTU, and pPolB polymerization palm domains but lacks the exonuclease domain and instead contains a superfamily 1 helicase domain. Analysis of the presence/absence and inactivation of the vOTU domains and replacement of pPolB with other DNA polymerases in eukaryotic preplasmiviricots enabled us to outline a complete scenario for their origin and evolution.

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Natural history of eukaryotic DNA viruses with double jelly-roll major capsid proteins

Krupovic,

Kuhn,

Fischer

et al. 2024

Preprint

Self Cite

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The phylum Preplasmiviricota (kingdom Bamfordvirae, realm Varidnaviria) is a broad assemblage of diverse viruses with comparatively short double-stranded DNA genomes (<50 kbp) that produce icosahedral capsids built from double jelly-roll major capsid proteins. Preplasmiviricots infect hosts from all cellular domains, testifying to their ancient origin and, in particular, are associated with six of the seven supergroups of eukaryotes. Preplasmiviricots comprise four major groups of viruses, namely, polintons, polinton-like viruses (PLVs), virophages, and adenovirids. We employed protein structure modeling and analysis to show that protein-primed DNA polymerases (pPolBs) of polintons, virophages, and cytoplasmic linear plasmids encompass an N-terminal domain homologous to the terminal proteins (TPs) of prokaryotic PRD1-like tectivirids and eukaryotic adenovirids that are involved in protein-primed replication initiation, followed by a viral ovarian tumor-like cysteine deubiquitinylase (vOTU) domain. The vOTU domain is likely responsible for the cleavage of the TP from the large pPolB polypeptide and is inactivated in adenovirids, in which TP is a separate protein. Many PLVs and transpovirons encode a distinct derivative of polinton-like pPolB that retains the TP, vOTU and pPolB polymerization palm domains but lacks the exonuclease domain and instead contains a supefamily 1 helicase domain. Analysis of the presence/absence and inactivation of the vOTU domains, and replacement of pPolB with other DNA polymerases in eukaryotic preplasmiviricots enabled us to outline a complete scenario for their origin and evolution.

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DNA Polymerase Diversity Reveals Multiple Incursions of Polintons During Nematode Evolution

Cited by 6 publications

References 86 publications

Widespread occurrence and diverse origins of polintoviruses influence lineage-specific genome dynamics in stony corals

Widespread occurrence and diverse origins of polintoviruses influence lineage-specific genome dynamics in stony corals

Natural history of eukaryotic DNA viruses with double jelly-roll major capsid proteins

Natural history of eukaryotic DNA viruses with double jelly-roll major capsid proteins

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