Comparative Analysis of the Circular and Highly Asymmetrical Marseilleviridae Genomes

Abstract

Marseilleviridae members are large dsDNA viruses with icosahedral particles 250 nm in diameter infecting Acanthamoeba. Their 340 to 390 kb genomes encode 450 to 550 protein-coding genes. Since the discovery of marseillevirus (the prototype of the family) in 2009, several strains were isolated from various locations, among which 13 are now fully sequenced. This allows the organization of their genomes to be deciphered through comparative genomics. Here, we first experimentally demonstrate that the Marseilleviridae genomes are circular. We then acknowledge a strong bias in sequence conservation, revealing two distinct genomic regions. One gathers most Marseilleviridae paralogs and has undergone genomic rearrangements, while the other, enriched in core genes, exhibits the opposite pattern. Most of the genes whose protein products compose the viral particles are located in the conserved region. They are also strongly biased toward a late gene expression pattern. We finally discuss the potential advantages of Marseilleviridae having a circular genome, and the possible link between the biased distribution of their genes and the transcription as well as DNA replication mechanisms that remain to be characterized.

Virus-encoded histone doublets are essential and form nucleosome-like structures

“…The time-course transcriptome analysis of A. castellanii cells infected by Marseillevirus was performed using the RNA-seq data from ( Rodrigues et al., 2020 ). We first annotated the Marseillevirus genome (accession GU071086) as described ( Blanca et al., 2020 ), as well as the A. castellanii Neff host genome (assembly GCA_000193105.1) using the Funannotate pipeline (version 1.7; https://github.com/nextgenusfs/funannotate ). We then mapped the RNA-seq reads corresponding to 30 min pi (ERR3528397), 1 h pi (ERR3528398), 2 h pi (ERR3528399), 4 h pi (ERR3528400), 5 h pi (ERR3528401), 6 h pi (ERR3528402), 8 h pi (ERR3528403), 10 h pi (ERR3528404) and 12 h pi (ERR3528405) to the host and viral transcripts using Bowtie ( Langmead and Salzberg, 2012 ) (version 2.3.4.1).…”

“…The time-course transcriptome analysis of A. castellanii cells infected by Marseillevirus was performed using the RNA-seq data from (Rodrigues et al, 2020). We first annotated the Marseillevirus genome (accession GU071086) as described (Blanca et al, 2020), as well as the A. castellanii Neff host genome (assembly GCA_000193105.1) using the Funannotate pipeline (version 1.7; https://github. com/nextgenusfs/funannotate).…”

The genomes of nucleocytoplasmic large DNA viruses: viral evolution writ large

“…Such an unequal distribution of core genes is also observed among NCLDVs with a circular genome [88]. Among the members of Marseilleviridae , the core gene regions are concentrated in a region covering one-third of the genome, in which genome rearrangements are nearly absent and primary sequence slightly more conserved [88].…”

“…The extremities of NCLDV genomes can also contain members of some conserved gene families, but their synteny and orientation are typically not conserved [87]. Such an unequal distribution of core genes is also observed among NCLDVs with a circular genome [88]. Among the members of Marseilleviridae , the core gene regions are concentrated in a region covering one-third of the genome, in which genome rearrangements are nearly absent and primary sequence slightly more conserved [88].…”

Marseilleviruses: An Update in 2021

“…A recent study conducted on the noumeavirus DNA confirmed by pulse-field gel electrophoresis and restriction digestion that its genome is circular ( Blanca et al, 2020 ). In addition, these authors conducted a comparative genomic study to analyze the organization of the marseillevirus genomes and reported an asymmetry in sequence conservation along these genomes.…”