Integrative omics analysis of <scp><i>Pseudomonas aeruginosa</i></scp> virus PA5oct highlights the molecular complexity of jumbo phages

Lood, Cédric; Danis-Wlodarczyk, Katarzyna; Blasdel, Bob; Jang, Ho Bin; Vandenheuvel, Dieter; Briers, Yves; Noben, Jean-Paul; Noort, Vera van; Drulis-Kawa, Zuzanna; Lavigne, Rob

doi:10.1111/1462-2920.14979

Cited by 35 publications

(28 citation statements)

References 93 publications

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“…However, jumbo phages have been rarely isolated by classical phage isolation method because of the large size of virions. Jumbo phages have mostly been isolated from Gram-negative bacteria, and only 11 jumbo phages have been reported from Gram-positive bacteria to date, most of which are Bacillus -infecting phages and one Staphylococcus infecting phage, S6 ( Uchiyama et al, 2014 ; Lood et al, 2020 ). Staphylococcus Jumbo phage S6 belongs to Myoviridae with genome size of approximately 270 kbp, but its genome has not been sequenced.…”

Section: Introductionmentioning

confidence: 99%

Characterization and Genomic Analysis of PALS2, a Novel Staphylococcus Jumbo Bacteriophage

et al. 2021

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Staphylococcus aureus is an important human pathogen that can be frequently encountered in clinical and food-processing surroundings. Among the various countermeasures, bacteriophages have been considered to be promising alternatives to antibiotics. In this study, the bacteriophage PALS2 was isolated from bird feces, and the genomic and biological characteristics of this phage were investigated. PALS2 was determined to belong to the Myoviridae family and exhibited extended host inhibition that persisted for up to 24 h with repeated bursts of 12 plaque-forming units/cell. The complete genome of PALS2 measured 268,746 base pairs (bp), indicating that PALS2 could be classified as a jumbo phage. The PALS2 genome contained 279 ORFs and 1 tRNA covering asparagine, and the majority of predicted PALS2 genes encoded hypothetical proteins. Additional genes involved in DNA replication and repair, nucleotide metabolism, and genes encoding multisubunit RNA polymerase were identified in the PALS2 genome, which is a common feature of typical jumbo phages. Comparative genomic analysis indicated that PALS2 is a phiKZ-related virus and is more similar to typical jumbo phages than to staphylococcal phages. Additionally, the effective antimicrobial activities of phage PALS2 suggest its possible use as a biocontrol agent in various clinical and food processing environments.

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Section: Introductionmentioning

confidence: 99%

Characterization and Genomic Analysis of PALS2, a Novel Staphylococcus Jumbo Bacteriophage

et al. 2021

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“…In contrast, many lytic phages have deadly mechanisms to shut down host gene expression and maximize expression of their own genes (5). These mechanisms often unfold in a concerted and controlled manner to give rise to tight temporal patterns of gene expression during infection, as has long been evidenced through targeted studies and more recently through global analyses such as RNA sequencing (RNA-seq) (6)(7)(8)(9)(10)(11)(12)(13).…”

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confidence: 99%

A Family of Viral Satellites Manipulates Invading Virus Gene Expression and Can Affect Cholera Toxin Mobilization

et al. 2020

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Many viruses possess temporally unfolding gene expression patterns aimed at subverting host defenses, commandeering host metabolism, and ultimately producing a large number of progeny virions. High-throughput omics tools, such as RNA sequencing (RNA-seq), have dramatically enhanced the resolution of expression patterns during infection. Less studied have been viral satellites, mobile genomes that parasitize viruses. By performing RNA-seq on infection time courses, we have obtained the first time-resolved transcriptomes for bacteriophage satellites during lytic infection. Specifically, we have acquired transcriptomes for the lytic Vibrio cholerae phage ICP1 and all five known variants of ICP1’s parasite, the phage inducible chromosomal island-like elements (PLEs). PLEs rely on ICP1 for both DNA replication and mobilization and abolish production of ICP1 progeny in infected cells. We investigated PLEs’ impact on ICP1 gene expression and found that PLEs did not broadly restrict or reduce ICP1 gene expression. A major exception occurred in ICP1’s capsid morphogenesis operon, which was downregulated by each of the PLE variants. Surprisingly, PLEs were also found to alter the gene expression of CTXΦ, the integrative phage that encodes cholera toxin and is necessary for virulence of toxigenic V. cholerae. One PLE, PLE1, upregulated CTXΦ genes involved in replication and integration and boosted CTXΦ mobility following induction of the SOS response. IMPORTANCE Viral satellites are found in all domains of life and can have profound fitness effects on both the viruses they parasitize and the cells they reside in. In this study, we have acquired the first RNA sequencing (RNA-seq) transcriptomes of viral satellites outside plants, as well as the transcriptome of the phage ICP1, a predominant predator of pandemic Vibrio cholerae. Capsid downregulation, previously observed in an unrelated phage satellite, is conserved among phage inducible chromosomal island-like elements (PLEs), suggesting that viral satellites are under strong selective pressure to reduce the capsid expression of their larger host viruses. Despite conserved manipulation of capsid expression, PLEs exhibit divergent effects on CTXΦ transcription and mobility. Our results demonstrate that PLEs can influence both their hosts’ resistance to phage and the mobility of virulence-encoding elements, suggesting that PLEs can play a substantial role in shaping Vibrio cholerae evolution.

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“…The genome sequences of many jumbo phages have few homologs when compared to previously annotated phages or other microorganisms and are even highly divergent when compared to each other (e.g. ФKZ and PA5oct, both infecting P. aeruginosa) (14,15,17,(20)(21)(22).…”

Section: Downloaded Frommentioning

confidence: 99%

“…The majority of them infect Gram-negative bacterial strains, including Escherichia, Pseudomonas, Aeromonas, Caulobacter, Erwinia, Vibrio, and Salmonella (14). Only 11 jumbo phages infect Gram-positive bacteria, mostly the Bacillus genus (15).…”

Section: Introductionmentioning

confidence: 99%

“…The majority of them infect Gram-negative bacterial strains, including Escherichia , Pseudomonas , Aeromonas , Caulobacter , Erwinia , Vibrio , and Salmonella strains ( 14 ). Only 11 jumbo phages infect Gram-positive bacteria, mostly the Bacillus genus ( 15 ). Most sequenced jumbo phages belong to the Myoviridae family, members of which have long contractile tails, while the rest belong to the Siphoviridae family, which have noncontractile tails.…”

Section: Introductionmentioning

confidence: 99%

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Intracellular Organization by Jumbo Bacteriophages

Guan

Bondy‐Denomy

2020

J Bacteriol

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Since their discovery over 100 years ago, the viruses that infect bacteria (bacteriophages) have been widely studied as model systems. Largely overlooked however, have been “jumbo phages”, with genome sizes ranging from 200 - 500 kbp. Jumbo phages generally have large virions with complex structures and a broad host spectrum. While the majority of jumbo phage genes are poorly functionally characterized, recent work has discovered many unique biological features, including a conserved tubulin homolog that coordinates a proteinaceous nucleus-like compartment that houses and segregates phage DNA. The tubulin spindle displays dynamic instability and centers the phage nucleus within the bacterial host during phage infection for optimal reproduction. The shell provides robust physical protection for the enclosed phage genomes against attack from bacterial DNA-targeting immune systems, thereby endowing jumbo phages with broad resistance. In this review, we focus on the current knowledge of the cytoskeletal elements and the specialized nuclear compartment derived from jumbo phages and highlight their importance in facilitating spatial and temporal organization over the viral life cycle. Additionally, we discuss the evolutionary relationships between jumbo phages and eukaryotic viruses, as well as the therapeutic potential and drawbacks of jumbo phages as antimicrobial agents in phage therapy.

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Integrative omics analysis of Pseudomonas aeruginosa virus PA5oct highlights the molecular complexity of jumbo phages

Cited by 35 publications

References 93 publications

Characterization and Genomic Analysis of PALS2, a Novel Staphylococcus Jumbo Bacteriophage

Characterization and Genomic Analysis of PALS2, a Novel Staphylococcus Jumbo Bacteriophage

A Family of Viral Satellites Manipulates Invading Virus Gene Expression and Can Affect Cholera Toxin Mobilization

Intracellular Organization by Jumbo Bacteriophages

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