Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate

Abstract

Virophages can parasitize giant DNA viruses and may provide adaptive anti-giant virus defense in unicellular eukaryotes. Under laboratory conditions, the virophage mavirus integrates into the nuclear genome of the marine flagellate Cafeteria burkhardae and reactivates upon superinfection with the giant virus CroV. In natural systems, however, the prevalence and diversity of host-virophage associations has not been systematically explored. Here, we report dozens of integrated virophages in four globally sampled C. burkhardae strains that constitute up to 2% of their host genomes. These endogenous mavirus-like elements (EMALEs) separated into eight types based on GC-content, nucleotide similarity, and coding potential and carried diverse promoter motifs implicating interactions with different giant viruses. Between host strains, some EMALE insertion loci were conserved indicating ancient integration events, whereas the majority of insertion sites were unique to a given host strain suggesting that EMALEs are active and mobile. Furthermore, we uncovered a unique association between EMALEs and a group of tyrosine recombinase retrotransposons, revealing yet another layer of parasitism in this nested microbial system. Our findings show that virophages are widespread and dynamic in wild Cafeteria populations, supporting their potential role in antiviral defense in protists.

Multiple waves of viral invasions in Symbiodiniaceae algal genomes

“…Furthermore, the putative inactivation of these elements by the host suggests that they were active when they were integrated into the genome, lending support to the second scenario (which produces viral elements that are “dead on arrival”). Moreover, the multiple, complete and incomplete copies of these viral genomes in Symbiodiniaceae, from different isolates and genera, suggests that viral endogenization is an ongoing process in these organisms, with a potentially rapid turnover of invasion and pseudogenization or activation and infection, similar to Mavirus virophage infection-integration cycles (Hackl et al 2021).…”

Simultaneous Giant Virus and Virophage Quantification Using Droplet Digital PCR

“…Giant viruses are complex viruses with large double stranded (ds) DNA genomes (up to 2500 kb) encoding hundreds of proteins [ 9 , 11 , 12 ], whereas virophages are small linear or circular dsDNA (17–30 kb) viruses. All virophages described so far are obligate parasites of giant viruses; some of them can also integrate into the host genome where they are transmitted vertically [ 5 , 13 , 14 ].For the production of progeny virions, the virophage requires the virus factory of the giant virus either during coinfection with the giant virus or following reactivation of the integrated virophage after infection of the host cell with the giant virus [ 7 , 15 ]. As virophages inhibit the production of giant virus particles, and favor host population survival [ 5 , 16 ], host–virus–virophage interactions can play a significant role in natural microbial community dynamics which might vary depending on ecological and environmental conditions.…”

“…Individual host cells do not benefit from inhibition of the giant virus, but the decrease in CroV production over time will reduce the number of new infection events and lead to increased host population density. While both giant viruses and virophages are widespread and diverse [ 14 , 19 , 20 ], their interactions are still poorly understood. For example, the abiotic and biotic conditions that trigger virophage reactivation are still unknown.…”

Integrated viral elements suggest the dual lifestyle of Tetraselmis spp. polinton-like viruses

“…They also encode DNA replication and integration proteins that were likely acquired independently in different virophage lineages (11). Virophages can integrate into the genome of the cellular or viral host (12)(13)(14), in which case they resemble Potintons, and and reactivates upon superinfection with a giant virus (8). Virophages can therefore have a dual life style combining a virus stage with an integrated stage The PLVs are also similar in size and genomic composition to the Polintons.…”