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Giant or Jumbo Phages

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

Deadline for manuscript submissions: closed (31 August 2020) | Viewed by 48565

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Special Issue Editors

Dr. Julie Thomas

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Guest Editor

Thomas H. Gosnell School of Life Sciences, College of Science, Rochester Institute of Technology, Rochester, NY, USA
Interests: giant phages; phage structure/assembly; genomics; genetics; proteomics; host–phage interactions
Special Issues, Collections and Topics in MDPI journals

Dr. Lindsay Black

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Guest Editor

Department of Biochemistry and Molecular Biology, University of Maryland School of Medicine, Baltimore, MD, USA
Interests: capsid condensed genome structure; viral nucleic acid motor translocation into a procapsid; host–phage interactions; phage epigenetic DNA modifications; phage genetics

Special Issue Information

Dear Colleagues,

Giant or jumbo phages are terms used to describe prokaryotic viruses with genomes >200 kb. These terms highlight how unusual this category of genome length is (it is longer than those of some endosymbiotic bacteria). Several giant phages have genomes that are extraordinary, nearly 500 kb (e.g., Phage G and Agrobacterium virus Atu_ph07), but it is unclear if this is the upper genome length limit. To date, all giant phages belong to the order Caudovirales, that is, they have a head with icosahedral symmetry and a tail. Most giant phages have a myoviral tail structure and some have a siphoviral tail. There are no known giant podoviruses. Despite all giant phages having counterparts to the major head components present in all tailed phages, at the genome level giant phage genomes represent an astonishing amount of genetic diversity. That is, the majority of genes in each giant phage genome are functionally unassigned. For some giant phages, it has been shown that some of these “additional” genes are used to create highly complex virions compared to those of phages with smaller genomes. Some giant phages have novel host infection strategies, suggesting that their “additional” genes can be an advantage with regard infection strategies and options. These data suggest that despite the additional cellular resources required to make a larger virion compared to a smaller virion, giant phages have evolved to be excellent parasites that can successfully compete for hosts in the environment.

Collectively, giant phages represent a wealth of research questions, including but not limited to their genomes, structure/assembly, novel infection strategies, ecology, evolution, and potential for applications ranging from clinical settings to industry and agriculture.

We encourage the submission of manuscripts that address these gaps in knowledge. We also wish to highlight that for this issue, we will consider T4 phage as an “honorary” giant phage and welcome the submission of research manuscripts on phages with T4-like core genes or strategies.

Dr. Julie Thomas
Dr. Lindsay Black
Guest Editors

Manuscript Submission Information

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Keywords

giant phage
jumbo phage
virion
host–phage interactions
evolution
ecology
phage therapy
applications

Published Papers (11 papers)

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Research

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42 pages, 39665 KiB

Open AccessArticle

Jumbo Phages: A Comparative Genomic Overview of Core Functions and Adaptions for Biological Conflicts

by Lakshminarayan M. Iyer, Vivek Anantharaman, Arunkumar Krishnan, A. Maxwell Burroughs and L. Aravind

Viruses 2021, 13(1), 63; https://doi.org/10.3390/v13010063 - 05 Jan 2021

Cited by 44 | Viewed by 7511

Abstract

Jumbo phages have attracted much attention by virtue of their extraordinary genome size and unusual aspects of biology. By performing a comparative genomics analysis of 224 jumbo phages, we suggest an objective inclusion criterion based on genome size distributions and present a synthetic overview of their manifold adaptations across major biological systems. By means of clustering and principal component analysis of the phyletic patterns of conserved genes, all known jumbo phages can be classified into three higher-order groups, which include both myoviral and siphoviral morphologies indicating multiple independent origins from smaller predecessors. Our study uncovers several under-appreciated or unreported aspects of the DNA replication, recombination, transcription and virion maturation systems. Leveraging sensitive sequence analysis methods, we identify novel protein-modifying enzymes that might help hijack the host-machinery. Focusing on host–virus conflicts, we detect strategies used to counter different wings of the bacterial immune system, such as cyclic nucleotide- and NAD⁺-dependent effector-activation, and prevention of superinfection during pseudolysogeny. We reconstruct the RNA-repair systems of jumbo phages that counter the consequences of RNA-targeting host effectors. These findings also suggest that several jumbo phage proteins provide a snapshot of the systems found in ancient replicons preceding the last universal ancestor of cellular life. Full article

(This article belongs to the Special Issue Giant or Jumbo Phages)

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12 pages, 4149 KiB

Open AccessArticle

Isolation and Characterization of Salmonella Jumbo-Phage pSal-SNUABM-04

by Jun Kwon, Sang Guen Kim, Hyoun Joong Kim, Sib Sankar Giri, Sang Wha Kim, Sung Bin Lee and Se Chang Park

Viruses 2021, 13(1), 27; https://doi.org/10.3390/v13010027 - 25 Dec 2020

Cited by 20 | Viewed by 3742

Abstract

The increasing emergence of antimicrobial resistance has become a global issue. Therefore, many researchers have attempted to develop alternative antibiotics. One promising alternative is bacteriophage. In this study, we focused on a jumbo-phage infecting Salmonella isolated from exotic pet markets. Using a Salmonella strain isolated from reptiles as a host, we isolated and characterized the novel jumbo-bacteriophage pSal-SNUABM-04. This phage was investigated in terms of its morphology, host infectivity, growth and lysis kinetics, and genome. The phage was classified as Myoviridae based on its morphological traits and showed a comparatively wide host range. The lysis efficacy test showed that the phage can inhibit bacterial growth in the planktonic state. Genetic analysis revealed that the phage possesses a 239,626-base pair genome with 280 putative open reading frames, 76 of which have a predicted function and 195 of which have none. By genome comparison with other jumbo phages, the phage was designated as a novel member of Machinavirus composed of Erwnina phages. Full article

(This article belongs to the Special Issue Giant or Jumbo Phages)

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18 pages, 48906 KiB

Open AccessArticle

Characterization of Novel Erwinia amylovora Jumbo Bacteriophages from Eneladusvirus Genus

by Sang Guen Kim, Sung Bin Lee, Sib Sankar Giri, Hyoun Joong Kim, Sang Wha Kim, Jun Kwon, Jungkum Park, Eunjung Roh and Se Chang Park

Viruses 2020, 12(12), 1373; https://doi.org/10.3390/v12121373 - 30 Nov 2020

Cited by 15 | Viewed by 3349

Abstract

Jumbo phages, which have a genome size of more than 200 kb, have recently been reported for the first time. However, limited information is available regarding their characteristics because few jumbo phages have been isolated. Therefore, in this study, we aimed to isolate and characterize other jumbo phages. We performed comparative genomic analysis of three Erwinia phages (pEa_SNUABM_12, pEa_SNUABM_47, and pEa_SNUABM_50), each of which had a genome size of approximately 360 kb (32.5% GC content). These phages were predicted to harbor 546, 540, and 540 open reading frames with 32, 34, and 35 tRNAs, respectively. Almost all of the genes in these phages could not be functionally annotated but showed high sequence similarity with genes encoded in Serratia phage BF, a member of Eneladusvirus. The detailed comparative and phylogenetic analyses presented in this study contribute to our understanding of the diversity and evolution of Erwinia phage and the genus Eneladusvirus. Full article

(This article belongs to the Special Issue Giant or Jumbo Phages)

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16 pages, 3283 KiB

Open AccessArticle

Maturation of Pseudo-Nucleus Compartment in P. aeruginosa, Infected with Giant phiKZ Phage

by Yana A. Danilova, Viktoriia V. Belousova, Andrey V. Moiseenko, Innokentii E. Vishnyakov, Maria V. Yakunina and Olga S. Sokolova

Viruses 2020, 12(10), 1197; https://doi.org/10.3390/v12101197 - 21 Oct 2020

Cited by 11 | Viewed by 4550

Abstract

The giant phiKZ phage infection induces the appearance of a pseudo-nucleus inside the bacterial cytoplasm. Here, we used RT-PCR, fluorescent in situ hybridization (FISH), electron tomography, and analytical electron microscopy to study the morphology of this unique nucleus-like shell and to demonstrate the distribution of phiKZ and bacterial DNA in infected Pseudomonas aeruginosa cells. The maturation of the pseudo-nucleus was traced in short intervals for 40 min after infection and revealed the continuous spatial separation of the phage and host DNA. Immediately after ejection, phage DNA was located inside the newly-identified round compartments; at a later infection stage, it was replicated inside the pseudo-nucleus; in the mature pseudo-nucleus, a saturated internal network of filaments was observed. This network consisted of DNA bundles in complex with DNA-binding proteins. On the other hand, the bacterial nucleoid underwent significant rearrangements during phage infection, yet the host DNA did not completely degrade until at least 40 min after phage application. Energy dispersive x-ray spectroscopy (EDX) analysis revealed that, during the infection, the sulfur content in the bacterial cytoplasm increased, which suggests an increase of methionine-rich DNA-binding protein synthesis, whose role is to protect the bacterial DNA from stress caused by infection. Full article

(This article belongs to the Special Issue Giant or Jumbo Phages)

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16 pages, 8644 KiB

Open AccessArticle

The Mottled Capsid of the Salmonella Giant Phage SPN3US, a Likely Maturation Intermediate with a Novel Internal Shell

by J. Bernard Heymann, Bing Wang, William W. Newcomb, Weimin Wu, Dennis C. Winkler, Naiqian Cheng, Erin R. Reilly, Ru-Ching Hsia, Julie A. Thomas and Alasdair C. Steven

Viruses 2020, 12(9), 910; https://doi.org/10.3390/v12090910 - 19 Aug 2020

Cited by 8 | Viewed by 3392

Abstract

“Giant” phages have genomes of >200 kbp, confined in correspondingly large capsids whose assembly and maturation are still poorly understood. Nevertheless, the first assembly product is likely to be, as in other tailed phages, a procapsid that subsequently matures and packages the DNA. The associated transformations include the cleavage of many proteins by the phage-encoded protease, as well as the thinning and angularization of the capsid. We exploited an amber mutation in the viral protease gene of the Salmonella giant phage SPN3US, which leads to the accumulation of a population of capsids with distinctive properties. Cryo-electron micrographs reveal patterns of internal density different from those of the DNA-filled heads of virions, leading us to call them “mottled capsids”. Reconstructions show an outer shell with T = 27 symmetry, an embellishment of the HK97 prototype composed of the major capsid protein, gp75, which is similar to some other giant viruses. The mottled capsid has a T = 1 inner icosahedral shell that is a complex network of loosely connected densities composed mainly of the ejection proteins gp53 and gp54. Segmentation of this inner shell indicated that a number of densities (~12 per asymmetric unit) adopt a “twisted hook” conformation. Large patches of a proteinaceous tetragonal lattice with a 67 Å repeat were also present in the cell lysate. The unexpected nature of these novel inner shell and lattice structures poses questions as to their functions in virion assembly. Full article

(This article belongs to the Special Issue Giant or Jumbo Phages)

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22 pages, 9876 KiB

Open AccessArticle

A Cut above the Rest: Characterization of the Assembly of a Large Viral Icosahedral Capsid

by Erin R. Reilly, Milky K. Abajorga, Cory Kiser, Nurul Humaira Mohd Redzuan, Zein Haidar, Lily E. Adams, Randy Diaz, Juliana A. Pinzon, André O. Hudson, Lindsay W. Black, Ru-Ching Hsia, Susan T. Weintraub and Julie A. Thomas

Viruses 2020, 12(7), 725; https://doi.org/10.3390/v12070725 - 05 Jul 2020

Cited by 7 | Viewed by 3776

Abstract

The head of Salmonella virus SPN3US is composed of ~50 different proteins and is unusual because within its packaged genome there is a mass (>40 MDa) of ejection or E proteins that enter the Salmonella cell. The assembly mechanisms of this complex structure are poorly understood. Previous studies showed that eight proteins in the mature SPN3US head had been cleaved by the prohead protease. In this study, we present the characterization of SPN3US prohead protease mutants using transmission electron microscopy and mass spectrometry. In the absence of the prohead protease, SPN3US head formation was severely impeded and proheads accumulated on the Salmonella inner membrane. This impediment is indicative of proteolysis being necessary for the release and subsequent DNA packaging of proheads in the wild-type phage. Proteomic analyses of gp245- proheads that the normal proteolytic processing of head proteins had not occurred. Assays of a recombinant, truncated form of the protease found it was active, leading us to hypothesize that the C-terminal propeptide has a role in targeting the protease into the prohead core. Our findings provide new evidence regarding the essential role of proteolysis for correct head assembly in this remarkable parasite. Full article

(This article belongs to the Special Issue Giant or Jumbo Phages)

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25 pages, 8382 KiB

Open AccessArticle

Pseudomonas Phage PaBG—A Jumbo Member of an Old Parasite Family

by Peter Evseev, Nina Sykilinda, Anna Gorshkova, Lidia Kurochkina, Rustam Ziganshin, Valentin Drucker and Konstantin Miroshnikov

Viruses 2020, 12(7), 721; https://doi.org/10.3390/v12070721 - 03 Jul 2020

Cited by 10 | Viewed by 3990

Abstract

Bacteriophage PaBG is a jumbo Myoviridae phage isolated from water of Lake Baikal. This phage has limited diffusion ability and thermal stability and infects a narrow range of Pseudomonas aeruginosa strains. Therefore, it is hardly suitable for phage therapy applications. However, the analysis of the genome of PaBG presents a number of insights into the evolutionary history of this phage and jumbo phages in general. We suggest that PaBG represents an ancient group distantly related to all known classified families of phages. Full article

(This article belongs to the Special Issue Giant or Jumbo Phages)

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10 pages, 1624 KiB

Open AccessArticle

The T4 TerL Prohead Packaging Motor Does Not Drive DNA Translocation by a Proposed Dehydration Mechanism

by Lindsay W. Black, Bingxue Yan and Krishanu Ray

Viruses 2020, 12(5), 522; https://doi.org/10.3390/v12050522 - 09 May 2020

Cited by 4 | Viewed by 2234

Abstract

A “DNA crunching” linear motor mechanism that employs a grip-and-release transient spring like compression of B- to A-form DNA has been found in our previous studies. Our FRET measurements in vitro show a decrease in distance from TerL to portal during packaging; furthermore, there is a decrease in distance between closely positioned dye pairs in the Y-stem of translocating Y-DNA that conforms to B- and A- structure. In normal translocation into the prohead the TerL motor expels all B-form tightly binding YOYO-1 dye that cannot bind A-form. The TerL motor cannot package A-form dsRNA. Our work reported here shows that addition of helper B form DNA:DNA (D:D) 20mers allows increased packaging of heteroduplex A-form DNA:RNA 20mers (D:R), evidence for a B- to A-form spring motor pushing duplex nucleic acid. A-form DNA:RNA 25mers, 30mers, and 35mers alone are efficiently packaged into proheads by the TerL motor showing that a proposed hypothetical dehydration motor mechanism operating on duplex substrates does not provide the packaging motor force. Taken together with our previous studies showing TerL motor protein motion toward the portal during DNA packaging, our present studies of short D:D and D:R duplex nucleic acid substrates strongly supports our previous evidence that the protein motor pushes rather than pulls or dehydrates duplex substrates to provide the translocation into prohead packaging force. Full article

(This article belongs to the Special Issue Giant or Jumbo Phages)

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Review

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18 pages, 1701 KiB

Open AccessReview

Phage phiKZ—The First of Giants

by Victor Krylov, Maria Bourkaltseva, Elena Pleteneva, Olga Shaburova, Sergey Krylov, Alexander Karaulov, Sergey Zhavoronok, Oxana Svitich and Vitaly Zverev

Viruses 2021, 13(2), 149; https://doi.org/10.3390/v13020149 - 20 Jan 2021

Cited by 22 | Viewed by 4716

Abstract

The paper covers the history of the discovery and description of phiKZ, the first known giant bacteriophage active on Pseudomonas aeruginosa. It also describes its unique features, especially the characteristic manner of DNA packing in the head around a cylinder-shaped structure (“inner body”), which probably governs an ordered and tight packaging of the phage genome. Important properties of phiKZ-like phages include a wide range of lytic activity and the blue opalescence of their negative colonies, and provide a background for the search and discovery of new P. aeruginosa giant phages. The importance of the phiKZ species and of other giant phage species in practical phage therapy is noted given their broad use in commercial phage preparations. Full article

(This article belongs to the Special Issue Giant or Jumbo Phages)

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13 pages, 2009 KiB

Open AccessReview

Multisubunit RNA Polymerases of Jumbo Bacteriophages

by Maria L. Sokolova, Inna Misovetc and Konstantin V. Severinov

Viruses 2020, 12(10), 1064; https://doi.org/10.3390/v12101064 - 23 Sep 2020

Cited by 22 | Viewed by 4104

Abstract

Prokaryotic viruses with DNA genome longer than 200 kb are collectively referred to as “jumbo phages”. Some representatives of this phylogenetically diverse group encode two DNA-dependent RNA polymerases (RNAPs)—a virion RNAP and a non-virion RNAP. In contrast to most other phage-encoded RNAPs, the jumbo phage RNAPs are multisubunit enzymes related to RNAPs of cellular organisms. Unlike all previously characterized multisubunit enzymes, jumbo phage RNAPs lack the universally conserved alpha subunits required for enzyme assembly. The mechanism of promoter recognition is also different from those used by cellular enzymes. For example, the AR9 phage non-virion RNAP requires uracils in its promoter and is able to initiate promoter-specific transcription from single-stranded DNA. Jumbo phages encoding multisubunit RNAPs likely have a common ancestor allowing making them a separate subgroup within the very diverse group of jumbo phages. In this review, we describe transcriptional strategies used by RNAP-encoding jumbo phages and describe the properties of characterized jumbo phage RNAPs. Full article

(This article belongs to the Special Issue Giant or Jumbo Phages)

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14 pages, 2584 KiB

Open AccessReview

In-Gel Isolation and Characterization of Large (and Other) Phages

by Philip Serwer and Elena T. Wright

Viruses 2020, 12(4), 410; https://doi.org/10.3390/v12040410 - 07 Apr 2020

Cited by 9 | Viewed by 3763

Abstract

We review some aspects of the rapid isolation of, screening for and characterization of jumbo phages, i.e., phages that have dsDNA genomes longer than 200 Kb. The first aspect is that, as plaque-supporting gels become more concentrated, jumbo phage plaques become smaller. Dilute agarose gels are better than conventional agar gels for supporting plaques of both jumbo phages and, prospectively, the even larger (>520 Kb genome), not-yet-isolated mega-phages. Second, dilute agarose gels stimulate propagation of at least some jumbo phages. Third, in-plaque techniques exist for screening for both phage aggregation and high-in-magnitude, negative average electrical surface charge density. The latter is possibly correlated with high phage persistence in blood. Fourth, electron microscopy of a thin section of a phage plaque reveals phage type, size and some phage life cycle information. Fifth, in-gel propagation is an effective preparative technique for at least some jumbo phages. Sixth, centrifugation through sucrose density gradients is a relatively non-destructive jumbo phage purification technique. These basics have ramifications in the development of procedures for (1) use of jumbo phages for phage therapy of infectious disease, (2) exploration of genomic diversity and evolution and (3) obtaining accurate metagenomic analyses. Full article

(This article belongs to the Special Issue Giant or Jumbo Phages)

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