This work was supported by the NASA Exobiology Program, grant 80NSSC17K0301 (I.D.L.H., G.W.K., E.L.T., A.A.P., and K.M.S.) and the NIH BUILD EXITO Program (A.M.). BUILD EXITO was supported by grants from the National Institutes of Health (UL1GM118964, RL5GM118963, and TL4GM118965) and the Portland State University Ronald E. McNair Scholars Program (E.L.T.), supported by grants from the U.S. Department of Education and Portland State University. The Antarctic field work was supported by the US National Science Foundation (NSF) under grant ANT-0944411, with logistics supplied by the US Antarctic Program. The freshwater work in New Zealand was supported by a grant (UC-E6007) from the American New Zealand Association (USA) awarded to P.Z.-R., C.G., J.S.H., and A.V. The green-lipped mussel work was supported by a grant from the Brian Mason Scientific & Technical Trust of New Zealand awarded to S.G. and A.V. EU-s Horizon 2020 Framework Program for Research and Innovation (‘Virus-X’, project no. 685778) supported F.E.
Viruses -- Evolution, Genetic transformation, Genetic recombination, Virology -- Environmental aspects, DNA viruses
The discovery of cruciviruses revealed the most explicit example of a common protein homologue between DNA and RNA viruses to date. Cruciviruses are a novel group of circular Rep-encoding single-stranded DNA (ssDNA) (CRESSDNA) viruses that encode capsid proteins that are most closely related to those encoded by RNA viruses in the family Tombusviridae. The apparent chimeric nature of the two core proteins encoded by crucivirus genomes suggests horizontal gene transfer of capsid genes between DNA and RNA viruses. Here, we identified and characterized 451 new crucivirus genomes and 10 capsid-encoding circular genetic elements through de novo assembly and mining of metagenomic data. These genomes are highly diverse, as demonstrated by sequence comparisons and phylogenetic analysis of subsets of the protein sequences they encode. Most of the variation is reflected in the replication-associated protein (Rep) sequences, and much of the sequence diversity appears to be due to recombination. Our results suggest that recombination tends to occur more frequently among groups of cruciviruses with relatively similar capsid proteins and that the exchange of Rep protein domains between cruciviruses is rarer than intergenic recombination. Additionally, we suggest members of the stramenopiles/alveolates/Rhizaria supergroup as possible crucivirus hosts. Altogether, we provide a comprehensive and descriptive characterization of cruciviruses.
de la Higuera I, Kasun GW, Torrance EL, Pratt AA, Maluenda A, Colombet J, Bisseux M, Ravet V, Dayaram A, Stainton D, Kraberger S, Zawar-Reza P, Goldstien S, Briskie JV, White R, Taylor H, Gomez C, Ainley DG, Harding JS, Fontenele RS, Schreck J, Ribeiro SG, Oswald SA, Arnold JM, Enault F, Varsani A, Stedman KM. 2020. Unveiling crucivirus diversity by mining metagenomic data. mBio 11:e01410-20. https://doi.org/10.1128/mBio.01410-20.