title: Membrane-assisted viral DNA ejection.
abstract: Genome packaging and delivery are fundamental steps in the replication cycle of all viruses. Icosahedral viruses with linear double-stranded DNA (dsDNA) usually package their genome into a preformed, rigid procapsid using the power generated by a virus-encoded packaging ATPase. The pressure and stored energy due to this confinement of DNA at a high density is assumed to drive the initial stages of genome ejection. Membrane-containing icosahedral viruses, such as bacteriophage PRD1, present an additional architectural complexity by enclosing their genome within an internal membrane vesicle. Upon adsorption to a host cell, the PRD1 membrane remodels into a proteo-lipidic tube that provides a conduit for passage of the ejected linear dsDNA through the cell envelope. Based on volume analyses of PRD1 membrane vesicles captured by cryo-electron tomography and modeling of the elastic properties of the vesicle, we propose that the internal membrane makes a crucial and active contribution during infection by maintaining the driving force for DNA ejection and countering the internal turgor pressure of the host. These novel functions extend the role of the PRD1 viral membrane beyond tube formation or the mere physical confinement of the genome. The presence and assistance of an internal membrane might constitute a biological advantage that extends also to other viruses that package their linear dsDNA to high density within an internal vesicle.
authors.affiliation: Structural Biology Unit, CIC bioGUNE, CIBERehd, Bizkaia Technology Park, 48160 Derio, Spain.
authors.forename: Isaac
authors.initials: I
authors.lastname: Santos-Pérez
authors.affiliation: Institute of Biotechnology and Department of Biosciences, Viikki Biocenter, University of Helsinki, P.O. Box 56, Viikinkaari 9B, 00014, Finland.
authors.forename: Hanna M
authors.initials: HM
authors.lastname: Oksanen
authors.affiliation: Institute of Biotechnology and Department of Biosciences, Viikki Biocenter, University of Helsinki, P.O. Box 56, Viikinkaari 9B, 00014, Finland.
authors.forename: Dennis H
authors.initials: DH
authors.lastname: Bamford
authors.affiliation: Unidad de Biofísica (CSIC, UPV/EHU) and Departamento de Bioquímica, Universidad del País Vasco, Bilbao, Spain.
authors.forename: Felix M
authors.initials: FM
authors.lastname: Goñi
authors.affiliation: Departament de Física de la Materia Condensada, Facultat de Física, Universitat de Barcelona, 08028 Barcelona, Spain.
authors.forename: David
authors.initials: D
authors.lastname: Reguera
authors.affiliation: Structural Biology Unit, CIC bioGUNE, CIBERehd, Bizkaia Technology Park, 48160 Derio, Spain; IKERBASQUE, Basque Foundation for Science, 48013 Bilbao, Spain. Electronic address: nabrescia@cicbiogune.es.
authors.forename: Nicola G A
authors.initials: NGA
authors.lastname: Abrescia
mesh_terms: D000251:Adenosine Triphosphatases / Q000378:metabolism; D025622:Bacteriophage PRD1 / Q000235:genetics; D002213:Capsid / Q000378:metabolism; D002462:Cell Membrane / Q000378:metabolism*; D004247:DNA / Q000235:genetics; D004279:DNA, Viral / Q000235:genetics*; D016679:Genome, Viral / Q000235:genetics; D014764:Viral Proteins / Q000235:genetics; D019065:Virus Assembly / Q000235:genetics
chemical_list: D004279:DNA, Viral; D014764:Viral Proteins; D004247:DNA; D000251:Adenosine Triphosphatases
keywords: Biophysical modeling; Cryo-electron tomography; Lipid-containing viruses; Membrane vesicle and properties; Models of viral DNA packaging; Viral DNA delivery