Genome of brown tide virus (AaV), the little giant of the Megaviridae, elucidates NCLDV genome expansion and host–virus coevolution

Abstract

Aureococcus anophagefferens causes economically and ecologically destructive "brown tides" in the United States, China and South Africa. Here we report the 370,920bp genomic sequence of AaV, a virus capable of infecting and lysing A. anophagefferens. AaV is a member of the nucleocytoplasmic large DNA virus (NCLDV) group, harboring 377 putative coding sequences and 8 tRNAs. Despite being an algal virus, AaV shows no phylogenetic affinity to the Phycodnaviridae family, to which most algae-infecting viruses belong. Core gene phylogenies, shared gene content and genome-wide similarities suggest AaV is the smallest member of the emerging clade "Megaviridae". The genomic architecture of AaV demonstrates that the ancestral virus had an even smaller genome, which expanded through gene duplication and assimilation of genes from diverse sources including the host itself - some of which probably modulate important host processes. AaV also harbors a number of genes exclusive to phycodnaviruses - reinforcing the hypothesis that Phycodna- and Mimiviridae share a common ancestor.

Comparative Genomics of Chrysochromulina Ericina Virus and Other Microalga-Infecting Large DNA Viruses Highlights Their Intricate Evolutionary Relationship with the Established Mimiviridae Family

“…The present analysis of the CeV genome adds to the mounting consensus that despite their large differences in gene content, particle size, host range, and ecology, a group of alga-infecting large dsDNA viruses (CeV, PgV, OLPV, and AaV) and the acanthamoeba-infecting Mimiviridae (genus, Mimivirus) belong to the same family and share an ancestor (3,7,8,13). This family also includes CroV (5), a virus that infects the heterotrophic stramenopile Cafeteria roenbergensis, as the sole member of the genus Cafeteriavirus.…”

“…3) suggests that the RPB2 paralogs originated from a single duplication that occurred after the divergence from the rest of the Mimiviridae. In addition, AaV exhibits two copies of RNA polymerase II large subunits (RPB1) (AaV_242 and AaV_320) (8).…”

“…Prior to defining these two genera, metagenomic studies had already hinted at the presence of mimivirus relatives in marine environments (6). The successful isolation and characterization of several of these viruses showed that they correspond to smaller icosahedral particles (140 to 180 nm in diameter) packing smaller dsDNA genomes (370 to 475 kb in length) (7)(8)(9). In core gene phylogenies, these viruses clearly cluster with the Mimiviridae, although they appear to constitute a distinct clade ( Fig.…”

“…In core gene phylogenies, these viruses clearly cluster with the Mimiviridae, although they appear to constitute a distinct clade ( Fig. 1) (1,2,7,8). This clade comprises only viruses infecting photosynthetic hosts (i.e., microalgae) from different taxa: haptophyceae for Phaeocystis globosa virus (PgV) and Haptolina ericina virus and stramenopile for Aureococcus anophagefferens virus (AaV).…”

In-depth study of Mollivirus sibericum , a new 30,000-y-old giant virus infecting Acanthamoeba

“…Their genomes are made of an adenine-thymine A+T-rich linear dsDNA molecule up to 1.26 Mb in length predicted to encode up to 1,120 proteins (3), including a transcription apparatus allowing them to replicate in the host's cytoplasm (4,5). The Mimiviridae family is still expanding (6) and diversifying with more distant and smaller representatives (both in terms of particle and genome size) that infect nonamoebal unicellular protists (7)(8)(9).…”