Clandestinovirus: A Giant Virus With Chromatin Proteins and a Potential to Manipulate the Cell Cycle of Its Host Vermamoeba vermiformis

Abstract

For several decades, the vast world of DNA viruses has been expanding constantly. Various discoveries in this field have broadened our knowledge and revealed that DNA viruses encode many functional features, which were once thought to be exclusive to cellular life. Here, we report the isolation of a giant virus named “clandestinovirus,” grown on the amoebal host Vermamoeba vermiformis. This virus was discovered in a mixed co-culture associated with another giant virus, Faustovirus ST1. Clandestinovirus possesses a linear dsDNA genome of 581,987 base pairs containing 617 genes. Phylogenetically, clandestinovirus is most closely related to Acanthamoeba castellanii medusavirus and was considered a member of the proposed Medusaviridae family. However, clandestinovirus genome is 65% larger than that of medusavirus, emphasizing the considerable genome size variation within this virus family. Functional annotation of the clandestinovirus genes suggests that the virus encodes four core histones. Furthermore, clandestinovirus appears to orchestrate the cell cycle and mitochondrial activities of the infected host by virtue of encoding a panel of protein kinases and phosphatases, and a suite of functionally diverse mitochondrial protein homologs, respectively. Collectively, these observations illuminate a strategy employed by clandestinovirus to optimize the intracellular environment for efficient virus propagation.

Particle Morphology of Medusavirus Inside and Outside the Cells Reveals a New Maturation Process of Giant Viruses

“…During the preparation of this report, we heard a new report that clandestinovirus is phylogenetically most closely related to medusavirus and was considered a member of the proposed Medusaviridae family ( 31 ). Like medusavirus, clandestinovirus possesses a genome encoding four core histones and one homolog of mitochondrial chaperon BCS1.…”

Diversity of Giant Viruses Infecting Vermamoeba vermiformis

“…Clandestinovirus (CLV), the first non-lytic isolate on V. vermiformis , was recently described ( Rolland et al, 2021 ). This virus was separated by a single cell microaspiration strategy ( Sahmi-Bounsiar et al, 2019 ) from a mixed co-culture associated with another giant virus (clandestinovirus ST1 and FV-ST1) collected from an environmental sample.…”

“…Clandestinovirus has an icosahedral capsid devoid of fibrils and has a virion size between 175 and 202 nm in diameter. It possesses a linear genome of 581,987 bp (43.5% G + C content) assembled in two scaffolds which encodes 617 open reading frames, corresponding to a coding density of 86% ( Rolland et al, 2021 ). In addition, it has one serine- and one histidine-like tRNAs.…”

“…Viral factories are observed 7–12 h.p.i, and at 16 h.p.i. The newly formed virions are discharged by exocytosis, which completes the replication cycle ( Rolland et al, 2021 ).…”

RNA Sequencing of Medusavirus Suggests Remodeling of the Host Nuclear Environment at an Early Infection Stage

“…Medusavirus, a giant virus that infects the amoeba Acanthamoeba castellanii , was isolated from a hot spring in Japan ( 2 ). Recently, a related virus, medusavirus stheno, was isolated from fresh water in Japan ( 19 ) and another distantly relate virus, clandestinovirus, was isolated from wastewater in France ( 20 ). These three viruses represent the proposed family “ Medusaviridae ” ( 2 ), which is distantly related to other giant virus families and forms an independent branch in the tree of the phylum Nucleocytoviricota .…”