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. 2021 Aug 10:12:715608.
doi: 10.3389/fmicb.2021.715608. eCollection 2021.

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

Clara Rolland  1   2 , Julien Andreani  1 , Dehia Sahmi-Bounsiar  1   2 , Mart Krupovic  3 , Bernard La Scola  1   2 , Anthony Levasseur  1   2   4
Affiliations

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

Clara Rolland et al. Front Microbiol. .

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.

Keywords: amoeba; clandestinovirus; giant virus; histones; mitochondria; nucleocytoviricota.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Replicative cycle of clandestinovirus. Scale bars are indicated on each panels. (A,B) Entry of the virus into Vermamoeba vermiformis by phagocytosis at 4 hpi. (C,D) Migration in the cytoplasm to the nucleus and entry into the host nucleus at 7 and 8 hpi. (E–G) Shows the replication of clandestinovirus in the nucleus which became a viral factory at 10 hpi (E) and 12 hpi (F,G). (H,I) Accumulation of mature viral particles at 11 and 12 hpi.
FIGURE 2
FIGURE 2
Description of clandestinovirus best hits obtained by blastp against the NCBI non-redundant database. (A) Total number of best hits by blast. (B) Description of the viruses’ best hits.
FIGURE 3
FIGURE 3
Phylogenetic tree of the DNA polymerase B sequences. The analysis was performed using the Maximum Likelihood method (ML) with a JTT substitution matrix in 1,000 replicates. Branch values lower than a bootstrap value of 0.5 were deleted. Colors were assigned for different group of viruses: blue for Mimiviruses and extended Mimiviridae; green for Pandoraviruses, Mollivirus sibericum, Emiliania huxleyi viruses (light green) and Phycodnaviridae (dark green); purple for groups of Asfarviridae, Faustoviruses, Pacmanvirus, and Kaumoabevirus; gray for Marseilleviridae; red for Orpheovirus, Solumvirus, Solivirus, Cedratviruses, and Pithovirus sibericum; and orange for Iridoviridae. Clandestinovirus is highlighted in bold and italic.
FIGURE 4
FIGURE 4
Conservation of specific modification sites in N-terminal tails of clandestinovirus histones. (A) Consensus. (B) Histone conserved modification sites in clandestinovirus.
FIGURE 5
FIGURE 5
Phylogenetic tree of the histone H3 of clandestinovirus. The analysis was performed using the ML method with a Jones-Taylor-Thornton (JTT) substitution matrix and 1,000 replicates. Branches with bootstrap support values below 0.50 were collapsed. Clandestinovirus is highlighted in bold and italic.
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