1. Multiple liquid crystalline geometries of highly compacted nucleic acid in a dsRNA virus
- Author
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Minna M. Poranen, F. de Haas, Juha T. Huiskonen, Jonathan M. Grimes, X. Sun, Abhay Kotecha, Frank DiMaio, K. El Omari, Serban L. Ilca, David I. Stuart, Molecular and Integrative Biosciences Research Programme, Molecular and Translational Virology, Helsinki Institute of Life Science HiLIFE, Helsinki Institute of Life Science HiLIFE, Joint Activities, and Laboratory of Structural Biology
- Subjects
Models, Molecular ,DOUBLE-HELICAL DNA ,viruses ,PROTEIN ,Genome, Viral ,02 engineering and technology ,ORGANIZATION ,Biology ,Genome ,BINDING-SITES ,Bacteriophage ,03 medical and health sciences ,chemistry.chemical_compound ,DNA Packaging ,STRANDED-RNA ,BACTERIOPHAGE PHI-6 ,Polymerase ,RNA, Double-Stranded ,030304 developmental biology ,Genomic organization ,11832 Microbiology and virology ,0303 health sciences ,Multidisciplinary ,IN-VITRO TRANSCRIPTION ,fungi ,POLYMERASE ,RNA ,CRYOELECTRON MICROSCOPY ,RNA-Dependent RNA Polymerase ,021001 nanoscience & nanotechnology ,biology.organism_classification ,Bacteriophage phi 6 ,Liquid Crystals ,Cell biology ,GENOME ,RNA silencing ,chemistry ,biology.protein ,Nucleic acid ,Nucleic Acid Conformation ,RNA, Viral ,1182 Biochemistry, cell and molecular biology ,0210 nano-technology ,DNA - Abstract
Characterizing the genome of mature virions is pivotal to understanding the highly dynamic processes of virus assembly and infection. Owing to the different cellular fates of DNA and RNA, the life cycles of double-stranded (ds) DNA and dsRNA viruses are dissimilar. In terms of nucleic acid packing, dsDNA viruses, which lack genome segmentation and intra-capsid transcriptional machinery, predominantly display single-spooled genome organizations(1-8). Because the release of dsRNA into the cytoplasm triggers host defence mechanisms(9), dsRNA viruses retain their genomes within a core particle that contains the enzymes required for RNA replication and transcription(10-12). The genomes of dsRNA viruses vary greatly in the degree of segmentation. In members of the Reoviridae family, genomes consist of 10-12 segments and exhibit a non-spooled arrangement mediated by RNA-dependent RNA polymerases(11-14). However, whether this arrangement is a general feature of dsRNA viruses remains unknown. Here, using cryo-electron microscopy to resolve the dsRNA genome structure of the tri-segmented bacteriophage Phi 6 of the Cystoviridae family, we show that dsRNA viruses can adopt a dsDNA-like single-spooled genome organization. We find that in this group of viruses, RNA-dependent RNA polymerases do not direct genome ordering, and the dsRNA can adopt multiple conformations. We build a model that encompasses 90% of the genome, and use this to quantify variation in the packing density and to characterize the different liquid crystalline geometries that are exhibited by the tightly compacted nucleic acid. Our results demonstrate that the canonical model for the packing of dsDNA can be extended to dsRNA viruses.
- Published
- 2019