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Discovery, Classification, and Early Research on the Lipid-Containing, Double-Stranded RNA...
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Discovery, Classification, and Early Research on the Lipid-Containing, Double-Stranded RNA Bacteriophage φ6

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Bacterial Viruses".

Deadline for manuscript submissions: 15 December 2024 | Viewed by 13967

Special Issue Editors

Dr. Paul Gottlieb

E-Mail Website
Guest Editor
CUNY School of medicine, Department of Molecular Cellular and Biomedical Science, City College of New York, New York, NY, USA
Interests: bacteriophage assembly and replication; use of virus-like particles for viral vaccine development
Aleksandra Alimova

E-Mail Website
Guest Editor Assistant
Department of Molecular, Cellular, and Biomedical Sciences, The City University of New York School of Medicine, New York, NY 10030, USA
Interests: bacteriophage assembly and replication; use of virus-like particles for viral vaccine development

Special Issue Information

Dear Colleagues,

Fifty years ago, the pseudomonad bacteriophage cystovirus φ6 was discovered in the laboratory headed by Anne Vidaver, PhD., at the Department of Plant Biology, University of Nebraska. The initial discovery elicited debate as the virion was found to be multilayered with an outer lipid envelope and to contain a genome consisting of three double-stranded RNA (dsRNA) segments. The unique (and surprising) architecture, which related the bacteriophage to the reovirus family, made it a useful model which offered simplicity to more complex systems. Consequently, a half-century of intensive research followed. Since that time and continuing until this day, φ6(and later discovered related types) has been found to be crucial in the elucidation of a wide array of mechanisms of viral assembly and replication. In particular, the multipartite genome segment selection process has been determined in order to correctly assemble a complete genome complement, both in regard to the RNA packaging signals and the physical interactions with the capsid proteins that insure accuracy and replication efficiency. The research was facilitated by pioneering work from the laboratory of Leonard Mindich, PhD., then working at the Public Health Research Institute (PHRI), first in New York City, New York and later in Newark, New Jersey. The Mindich laboratory determined the gene linkage groups, confirming the presence of three unique dsRNA segments, and continued by providing the entire φ6 genome sequence and gene identification. Further studies from multiple laboratories worldwide identified additional cystovirus types, allowing significant studies to be conducted that assessed the structure of the bacteriophage packaging proteins and the dynamic changes they undergo during genome packaging and transcription. The papers in this Special Issue review these discoveries and summarize current research efforts, including suggestions for future studies.

Dr. Paul Gottlieb
Guest Editor

Aleksandra Alimova
Guest Editor Assistant

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Keywords

  • procapsid
  • nucleocapsid
  • polymerase complex
  • assembly
  • replication
  • recombination
  • packaging10

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Published Papers (7 papers)

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Editorial

Jump to: Review

8 pages, 3095 KiB  
Editorial
The Establishment of the ϕ6 Genome Packaging Assay
by Paul Gottlieb and Aleksandra Alimova
Viruses 2024, 16(1), 22; https://doi.org/10.3390/v16010022 - 22 Dec 2023
Viewed by 985
Abstract
This editorial describes the efforts to establish a genome packaging assay for the ϕ6 bacteriophage, which were performed in the laboratory of Leonard Mindich, Ph [...] Full article
(This article belongs to the Special Issue Discovery, Classification, and Early Research on the Lipid-Containing, Double-Stranded RNA Bacteriophage φ6)
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Review

Jump to: Editorial

17 pages, 1717 KiB  
Review
Experimental Evolution Studies in Φ6 Cystovirus
by Sonia Singhal, Akiko K. Balitactac, Aruna G. Nayagam, Parnian Pour Bahrami, Sara Nayeem and Paul E. Turner
Viruses 2024, 16(6), 977; https://doi.org/10.3390/v16060977 - 18 Jun 2024
Cited by 2 | Viewed by 1225
Abstract
Experimental evolution studies, in which biological populations are evolved in a specific environment over time, can address questions about the nature of spontaneous mutations, responses to selection, and the origins and maintenance of novel traits. Here, we review more than 30 years of [...] Read more.
Experimental evolution studies, in which biological populations are evolved in a specific environment over time, can address questions about the nature of spontaneous mutations, responses to selection, and the origins and maintenance of novel traits. Here, we review more than 30 years of experimental evolution studies using the bacteriophage (phage) Φ6 cystovirus. Similar to many lab-studied bacteriophages, Φ6 has a high mutation rate, large population size, fast generation time, and can be genetically engineered or cryogenically frozen, which facilitates its rapid evolution in the laboratory and the subsequent characterization of the effects of its mutations. Moreover, its segmented RNA genome, outer membrane, and capacity for multiple phages to coinfect a single host cell make Φ6 a good non-pathogenic model for investigating the evolution of RNA viruses that infect humans. We describe experiments that used Φ6 to address the fitness effects of spontaneous mutations, the consequences of evolution in the presence of coinfection, the evolution of host ranges, and mechanisms and consequences of the evolution of thermostability. We highlight open areas of inquiry where further experimentation on Φ6 could inform predictions for pathogenic viruses. Full article
(This article belongs to the Special Issue Discovery, Classification, and Early Research on the Lipid-Containing, Double-Stranded RNA Bacteriophage φ6)
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17 pages, 2143 KiB  
Review
Utilization of Bacteriophage phi6 for the Production of High-Quality Double-Stranded RNA Molecules
by Alesia A. Levanova and Minna M. Poranen
Viruses 2024, 16(1), 166; https://doi.org/10.3390/v16010166 - 22 Jan 2024
Cited by 1 | Viewed by 1993
Abstract
Double-stranded RNA (dsRNA) molecules are mediators of RNA interference (RNAi) in eukaryotic cells. RNAi is a conserved mechanism of post-transcriptional silencing of genes cognate to the sequences of the applied dsRNA. RNAi-based therapeutics for the treatment of rare hereditary diseases have recently emerged, [...] Read more.
Double-stranded RNA (dsRNA) molecules are mediators of RNA interference (RNAi) in eukaryotic cells. RNAi is a conserved mechanism of post-transcriptional silencing of genes cognate to the sequences of the applied dsRNA. RNAi-based therapeutics for the treatment of rare hereditary diseases have recently emerged, and the first sprayable dsRNA biopesticide has been proposed for registration. The range of applications of dsRNA molecules will likely expand in the future. Therefore, cost-effective methods for the efficient large-scale production of high-quality dsRNA are in demand. Conventional approaches to dsRNA production rely on the chemical or enzymatic synthesis of single-stranded (ss)RNA molecules with a subsequent hybridization of complementary strands. However, the yield of properly annealed biologically active dsRNA molecules is low. As an alternative approach, we have developed methods based on components derived from bacteriophage phi6, a dsRNA virus encoding RNA-dependent RNA polymerase (RdRp). Phi6 RdRp can be harnessed for the enzymatic production of high-quality dsRNA molecules. The isolated RdRp efficiently synthesizes dsRNA in vitro on a heterologous ssRNA template of any length and sequence. To scale up dsRNA production, we have developed an in vivo system where phi6 polymerase complexes produce target dsRNA molecules inside Pseudomonas cells. Full article
(This article belongs to the Special Issue Discovery, Classification, and Early Research on the Lipid-Containing, Double-Stranded RNA Bacteriophage φ6)
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17 pages, 12699 KiB  
Review
Structural Studies of Bacteriophage Φ6 and Its Transformations during Its Life Cycle
by J. Bernard Heymann
Viruses 2023, 15(12), 2404; https://doi.org/10.3390/v15122404 - 11 Dec 2023
Cited by 1 | Viewed by 1959
Abstract
From the first isolation of the cystovirus bacteriophage Φ6 from Pseudomonas syringae 50 years ago, we have progressed to a better understanding of the structure and transformations of many parts of the virion. The three-layered virion, encapsulating the tripartite double-stranded RNA (dsRNA) genome, [...] Read more.
From the first isolation of the cystovirus bacteriophage Φ6 from Pseudomonas syringae 50 years ago, we have progressed to a better understanding of the structure and transformations of many parts of the virion. The three-layered virion, encapsulating the tripartite double-stranded RNA (dsRNA) genome, breaches the cell envelope upon infection, generates its own transcripts, and coopts the bacterial machinery to produce its proteins. The generation of a new virion starts with a procapsid with a contracted shape, followed by the packaging of single-stranded RNA segments with concurrent expansion of the capsid, and finally replication to reconstitute the dsRNA genome. The outer two layers are then added, and the fully formed virion released by cell lysis. Most of the procapsid structure, composed of the proteins P1, P2, P4, and P7 is now known, as well as its transformations to the mature, packaged nucleocapsid. The outer two layers are less well-studied. One additional study investigated the binding of the host protein YajQ to the infecting nucleocapsid, where it enhances the transcription of the large RNA segment that codes for the capsid proteins. Finally, I relate the structural aspects of bacteriophage Φ6 to those of other dsRNA viruses, noting the similarities and differences. Full article
(This article belongs to the Special Issue Discovery, Classification, and Early Research on the Lipid-Containing, Double-Stranded RNA Bacteriophage φ6)
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13 pages, 1217 KiB  
Review
Diversity and Current Classification of dsRNA Bacteriophages
by Sari Mäntynen, Meri M. Salomaa and Minna M. Poranen
Viruses 2023, 15(11), 2154; https://doi.org/10.3390/v15112154 - 25 Oct 2023
Cited by 2 | Viewed by 2477
Abstract
Half a century has passed since the discovery of Pseudomonas phage phi6, the first enveloped dsRNA bacteriophage to be isolated. It remained the sole known dsRNA phage for a quarter of a century and the only recognised member of the Cystoviridae family until [...] Read more.
Half a century has passed since the discovery of Pseudomonas phage phi6, the first enveloped dsRNA bacteriophage to be isolated. It remained the sole known dsRNA phage for a quarter of a century and the only recognised member of the Cystoviridae family until the year 2018. After the initial discovery of phi6, additional dsRNA phages have been isolated from globally distant locations and identified in metatranscriptomic datasets, suggesting that this virus type is more ubiquitous in nature than previously acknowledged. Most identified dsRNA phages infect Pseudomonas strains and utilise either pilus or lipopolysaccharide components of the host as the primary receptor. In addition to the receptor-mediated strictly lytic lifestyle, an alternative persistent infection strategy has been described for some dsRNA phages. To date, complete genome sequences of fourteen dsRNA phage isolates are available. Despite the high sequence diversity, similar sets of genes can typically be found in the genomes of dsRNA phages, suggesting shared evolutionary trajectories. This review provides a brief overview of the recognised members of the Cystoviridae virus family and related dsRNA phage isolates, outlines the current classification of dsRNA phages, and discusses their relationships with eukaryotic RNA viruses. Full article
(This article belongs to the Special Issue Discovery, Classification, and Early Research on the Lipid-Containing, Double-Stranded RNA Bacteriophage φ6)
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21 pages, 3035 KiB  
Review
Discovery and Classification of the φ6 Bacteriophage: An Historical Review
by Paul Gottlieb and Aleksandra Alimova
Viruses 2023, 15(6), 1308; https://doi.org/10.3390/v15061308 - 31 May 2023
Cited by 3 | Viewed by 2219
Abstract
The year 2023 marks the fiftieth anniversary of the discovery of the bacteriophage φ6. The review provides a look back on the initial discovery and classification of the lipid-containing and segmented double-stranded RNA (dsRNA) genome-containing bacteriophage—the first identified cystovirus. The historical discussion describes, [...] Read more.
The year 2023 marks the fiftieth anniversary of the discovery of the bacteriophage φ6. The review provides a look back on the initial discovery and classification of the lipid-containing and segmented double-stranded RNA (dsRNA) genome-containing bacteriophage—the first identified cystovirus. The historical discussion describes, for the most part, the first 10 years of the research employing contemporary mutation techniques, biochemical, and structural analysis to describe the basic outline of the virus replication mechanisms and structure. The physical nature of φ6 was initially controversial as it was the first bacteriophage found that contained segmented dsRNA, resulting in a series of early publications that defined the unusual genomic quality. The technology and methods utilized in the initial research (crude by current standards) meant that the first studies were quite time-consuming, hence the lengthy period covered by this review. Yet when the data were accepted, the relationship to the reoviruses was apparent, launching great interest in cystoviruses, research that continues to this day. Full article
(This article belongs to the Special Issue Discovery, Classification, and Early Research on the Lipid-Containing, Double-Stranded RNA Bacteriophage φ6)
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26 pages, 4539 KiB  
Review
Heterologous RNA Recombination in the Cystoviruses φ6 and φ8: A Mechanism of Viral Variation and Genome Repair
by Paul Gottlieb and Aleksandra Alimova
Viruses 2022, 14(11), 2589; https://doi.org/10.3390/v14112589 - 21 Nov 2022
Cited by 3 | Viewed by 2246
Abstract
Recombination and mutation of viral genomes represent major mechanisms for viral evolution and, in many cases, moderate pathogenicity. Segmented genome viruses frequently undergo reassortment of the genome via multiple infection of host organisms, with influenza and reoviruses being well-known examples. Specifically, major genomic [...] Read more.
Recombination and mutation of viral genomes represent major mechanisms for viral evolution and, in many cases, moderate pathogenicity. Segmented genome viruses frequently undergo reassortment of the genome via multiple infection of host organisms, with influenza and reoviruses being well-known examples. Specifically, major genomic shifts mediated by reassortment are responsible for radical changes in the influenza antigenic determinants that can result in pandemics requiring rapid preventative responses by vaccine modifications. In contrast, smaller mutational changes brought about by the error-prone viral RNA polymerases that, for the most part, lack a replication base mispairing editing function produce small mutational changes in the RNA genome during replication. Referring again to the influenza example, the accumulated mutations—known as drift—require yearly vaccine updating and rapid worldwide distribution of each new formulation. Coronaviruses with a large positive-sense RNA genome have long been known to undergo intramolecular recombination likely mediated by copy choice of the RNA template by the viral RNA polymerase in addition to the polymerase-based mutations. The current SARS-CoV-2 origin debate underscores the importance of understanding the plasticity of viral genomes, particularly the mechanisms responsible for intramolecular recombination. This review describes the use of the cystovirus bacteriophage as an experimental model for recombination studies in a controlled manner, resulting in the development of a model for intramolecular RNA genome alterations. The review relates the sequence of experimental studies from the laboratory of Leonard Mindich, PhD at the Public Health Research Institute—then in New York City—and covers a period of approximately 12 years. Hence, this is a historical scientific review of research that has the greatest relevance to current studies of emerging RNA virus pathogens. Full article
(This article belongs to the Special Issue Discovery, Classification, and Early Research on the Lipid-Containing, Double-Stranded RNA Bacteriophage φ6)
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