Morphological and Taxonomic Properties of the Newly Isolated Cotonvirus japonicus , a New Lineage of the Subfamily Megavirinae

Abstract

Since 2003, various viruses from the subfamily Megavirinae in the family Mimiviridae have been isolated worldwide, including icosahedral mimiviruses and tailed tupanviruses. To date, the evolutionary relationship between tailed and non-tailed mimiviruses has not yet been elucidated. Here, we present the genomic and morphological features of a newly isolated giant virus, Cotonvirus japonicus (cotonvirus), belonging to the family Mimiviridae. It contains a linear double-stranded DNA molecule of 1.47 Mb, the largest among the reported viruses in the subfamily Megavirinae , excluding tupanviruses. Among its 1,306 predicted open reading frames, 1,149 (88.0%) were homologous to those of the family Mimiviridae . Several nucleocytoplasmic large DNA virus (NCLDV) core genes, aminoacyl-tRNA synthetase genes, and the host specificity of cotonvirus were highly similar to those of Mimiviridae lineages A, B, and C; however, lineage A was slightly closer to cotonvirus than to the others. Moreover, based on its genome size, the presence of two copies of 18S rRNA-like sequences, and period of infection cycle, cotonvirus is the most similar to the tupanviruses among the icosahedral mimiviruses. Interestingly, the cotonvirus utilizes Golgi apparatus-like vesicles for virion factory (VF) formation. Overall, we showed that cotonvirus is a novel lineage of the subfamily Megavirinae . Our findings support the diversity of icosahedral mimiviruses and provide mechanistic insights into the replication, VF formation, and evolution of the subfamily Mimivirinae . Importance We have isolated a new virus of an independent lineage belonging to the family Mimiviridae , subfamily Megavirinae , from the fresh water of a canal in Japan, named cotonvirus. In a proteomic tree, this new nucleocytoplasmic large DNA virus (NCLDV) is phylogenetically placed at the root of three lineages of the subfamily Megavirinae —lineages A (mimivirus), B (moumouvirus), and C (megavirus). Multiple genomic and phenotypic features of cotonvirus are similar to those of tupanviruses, rather than the A, B, or C lineages, and other genomic features and host specificity of cotonvirus are similar to those of the latter than the former. These results suggest that cotonvirus is a unique virus, with chimeric features of existing viruses of Megavirinae and uses Golgi apparatus-like vesicles of the host cells for virion factory (VF) formation. Thus, cotonvirus can provide novel insights into the evolution of mimiviruses and the underlying mechanisms of VF formation.

Kinetic Analysis of Acanthamoeba castellanii Infected with Giant Viruses Quantitatively Revealed Process of Morphological and Behavioral Changes in Host Cells

“…Various CPEs have been reported, including cell rounding, lysis, aggregation, and cyst formation ( 8 – 12 ). Most of the viruses that infect Acanthamoeba cause cell rounding in the late stages of infection, and then some viruses lead to cell lysis ( 8 , 10 – 13 ). It has also been reported that tupanvirus ( Mimiviridae ) and hokutovirus ( Marseilleviridae ) cause cell aggregation before cell rounding ( 9 , 10 ).…”

Hybrid Sequencing Resolved Inverted Terminal Repeats in the Genome of Megavirus Baoshan

“…To estimate the phylogenetic position of Me. baoshan in the family Mimiviridae , molecular phylogenetic analysis was performed based on NCLDV core genes, including major capsid protein, family B DNA polymerase, D5-like primase-helicase, transcription factor S-II, and virion packaging ATPase ( Assis et al, 2017 ; Abrahão et al, 2018 ; Takahashi et al, 2021 ). Me.…”

“…Members of Mimiviridae can be divided into several lineages, including lineage A (represented by APMV, La Scola et al, 2003 ), B (Acanthamoeba polyphaga moumouvirus, Yoosuf et al, 2012 ), C (Megavirus chiliensis, Arslan et al, 2011 ), and Tupanvirus ( Abrahão et al, 2018 ), based on the phylogenetic analysis of conserved genes, like major capsid protein, family B DNA polymerase, D5-like primase-helicase, etc. New lineage has been proposed due to the isolation of new viruses ( Takahashi et al, 2021 ). Using different gene or gene set may result in slightly different topology in the phylogenic tree, but the lineage classification remains unchanged ( Arslan et al, 2011 ; Yoosuf et al, 2012 ; Assis et al, 2017 ; Abrahão et al, 2018 ; Takahashi et al, 2021 ).…”

“…New lineage has been proposed due to the isolation of new viruses ( Takahashi et al, 2021 ). Using different gene or gene set may result in slightly different topology in the phylogenic tree, but the lineage classification remains unchanged ( Arslan et al, 2011 ; Yoosuf et al, 2012 ; Assis et al, 2017 ; Abrahão et al, 2018 ; Takahashi et al, 2021 ). Mimivirus had a large and complex genome with a relatively conserved central region and highly diversified terminal areas ( Arslan et al, 2011 ; Yoosuf et al, 2012 ).…”

The Astounding World of Glycans from Giant Viruses

“…44 The VF in which nucleic acids accumulate due to active transcription and replication increases in size and neosynthesized virions start budding at its periphery, recycling host cell membranes derived from the ER, 44,79,80 or Golgi compartments, as recently described for Cotonvirus (clade E). 81 The last step in virion maturation, after genome loading into the nucleoid, is the addition to the capsid of the fibril layer, which comprises many proteins and two different polysaccharides (section 3.2.2). 80,82 Hundreds of neosynthesized virions are released after cell lysis.…”