Sheep in wolves’ clothing: Temperate T7-like bacteriophages and the origins of the Autographiviridae

Boeckman, Justin; Korn, Abby; Yao, Guichun; Aravind, R.; Gonzalez, Carlos F.; Gill, Jason J.

doi:10.1016/j.virol.2022.01.013

Cited by 16 publications

(36 citation statements)

References 76 publications

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“…The presented analysis is congruent with the recent taxonomic ratification of autographiviruses [ 96 ] and previous comparative studies of the Autographiviridae family that focused mostly on phylogenetic analyses of individually characterized viruses in relation to their closest relatives based on the major capsid protein [ 113 , 114 , 115 , 116 ] terminase large subunit [ 93 , 113 , 115 , 116 , 117 , 118 ], RNA polymerase [ 91 , 114 , 116 , 117 , 118 ], DNA polymerase [ 23 , 114 , 116 , 119 ], tail tubular proteins [ 120 ], or head–tail connector [ 114 ] used as marker proteins, as well as with the analyses of the whole proteome of some groups of Autographiviridae representatives known at that time [ 22 , 84 , 121 ] using different databases (RefSeqv88, NCBI GenBank, and ACLAME, respectively). However, our global approach is the first to use a much larger number of phages (over 17,470 available in the INPHARED database) than was included in previous studies, adding recently discovered autographiviruses and those from metagenomic studies.…”

Section: Resultsmentioning

confidence: 99%

“…Recently, an autographivirus Pasto was found to be able to enter the lysogenic cycle in its host Agrobacterium sp. [ 22 ], making it the first active temperate Autographiviridae phage and starting point for the identification of T7-like prophages in a wide variety of Gram-negative and several Gram-positive bacterial genomes. Another functional temperate Autographiviridae was Teseptimavirus S2B, infecting the Caulobacter crescentus strain CB15 [ 23 ].…”

Section: Introductionmentioning

confidence: 99%

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Characterization of Three Novel Virulent Aeromonas Phages Provides Insights into the Diversity of the Autographiviridae Family

Bujak

Decewicz

Kitowicz

et al. 2022

Viruses

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In this study, we isolated and characterized three novel virulent Autographiviridae bacteriophages, vB_AspA_Bolek, vB_AspA_Lolek, and vB_AspA_Tola, which infect different Aeromonas strains. These three host–pathogen pairs were derived from the same sampling location—the arsenic-containing microbial mats of the Zloty Stok gold mine. Functional analysis showed they are psychrotolerant (4–25 °C), albeit with a much wider temperature range of propagation for the hosts (≤37 °C). Comparative genomic analyses revealed a high nucleotide and amino acid sequence similarity of vB_AspA_Bolek and vB_AspA_Lolek, with significant differences exclusively in the C-terminal region of their tail fibres, which might explain their host range discrimination. The protein-based phage network, together with a phylogenetic analysis of the marker proteins, allowed us to assign vB_AspA_Bolek and vB_AspA_Lolek to the Beijerinckvirinae and vB_AspA_Tola to the Colwellvirinae subfamilies, but as three novel species, due to their low nucleotide sequence coverage and identity with other known phage genomes. Global comparative analysis showed that the studied phages are also markedly different from most of the 24 Aeromonas autographiviruses known so far. Finally, this study provides in-depth insight into the diversity of the Autographiviridae phages and reveals genomic similarities between selected groups of this family as well as between autographiviruses and their relatives of other Caudoviricetes families.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Characterization of Three Novel Virulent Aeromonas Phages Provides Insights into the Diversity of the Autographiviridae Family

Bujak

Decewicz

Kitowicz

et al. 2022

Viruses

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“…Identity <80%). In addition, unlike other T7-like phages infecting P. aeruginosa , the LUZ100 genome encodes an integrase gene (tyrosine site-specific recombinase) upstream of the RNA polymerase gene, suggesting that this phage could lysogenize its host cells (14, 15).…”

Section: Resultsmentioning

confidence: 99%

“…Directly upstream of the integrase, LUZ100 encodes a MarR-like transcriptional regulator. This regulator has been identified in several integrase-coding T7-like phages and was recently proposed to be involved in their lytic/lysogeny decision (8, 14, 15). The ONT-cappable-seq data shows that the MarR-like regulator and the integrase are co-transcribed in an operon from host-specific promoter P3.…”

Section: Resultsmentioning

confidence: 99%

“…The phage RNAP is key to complete a lytic infection cycle, and the regulation of the polymerase is proposed to be intertwined with the MarR-based transcriptional regulation in some of the temperate T7-like phages (14). During lysogeny, the MarR regulator is hypothesized to repress phage RNAP expression through recognition of specific binding sites sequences that flank the promoter sequence upstream the RNAP (14). Interestingly, in case of LUZ100, the location of phage-specific promoter ϕ1, encoded directly upstream of the RNAP, raises questions on how the RNAP becomes initially activated.…”

Section: Resultsmentioning

confidence: 99%

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Transcriptomics-driven characterisation of novel T7-like temperate Pseudomonas phage LUZ100

Putzeys

Poppeliers

Boon

et al. 2022

Preprint

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The Autographiviridae is a diverse yet distinct family of bacterial viruses marked by a strictly lytic lifestyle and a generally conserved genome organization. We here characterise Pseudomonas aeruginosa phage LUZ100, a distant relative of type phage T7. LUZ100 is a podovirus with a limited host range and identified LPS as the likely phage receptor. Interestingly, infection dynamics of LUZ100 indicated moderate adsorption rates and low virulence, hinting towards temperate behavior. This hypothesis was supported by genomic analysis, which showed that LUZ100 shares the conventional T7-like genome organization, yet encodes key genes associated with a temperate lifestyle. To unravel the peculiar characteristics of LUZ100, ONT-cappable-seq transcriptomics analysis was performed. This data generated a bird’s-eye view of the LUZ100 transcriptome and enabled the discovery of key regulatory elements, antisense RNA, and transcriptional unit structures. The transcriptional map of LUZ100 also allowed us to identify new RNAP-promoter pairs that can form the basis for biotechnological parts and tools for new synthetic transcription regulation circuitry. The ONT-cappable-seq data revealed that the LUZ100 integrase and a MarR-like regulator (proposed to be involved in the lytic/lysogeny decision), are actively co-transcribed in an operon. In addition, the presence of a phage-specific promoter transcribing the phage-encoded RNA polymerase, raises questions on the regulation of this polymerase, and suggests it is interwoven with the MarR-based regulation. This transcriptomics-driven characterisation of LUZ100 supports the increasing evidence that T7-like phages should not straightforwardly be marked as having a strictly lytic lifecycle.

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Isolation, characterization, and evaluation of putative new bacteriophages for controlling bacterial spot on tomato in Brazil

de Sousa,

Janssen,

Rosa

et al. 2023

Arch Virol

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Bacterial spot is a highly damaging tomato disease caused by several species of the genus Xanthomonas. Bacteriophages have been studied for their potential use as a biological control method for bacterial diseases. Parte superior do formulário In the present study, bacteriophages were obtained from soil and tomato leaves in commercial elds in Brazil with the aim of obtaining biological control agents against bacterial spot. Phage isolation was carried out through co-cultivation with isolates of Xanthomonas euvesicatoria pv. perforans (Xp), which was prevalent in the collected areas. In the host range evaluation, no phage was able to induce a lytic cycle in all bacterial isolates. Then, in the in vivo tests, when Xpisolates were sensitive to the used phages, we observed that the prior application of phage suspension led to a reduction in the severity of the disease. The disease control level provided by phage application was equal to or greater than that obtained by the use of copper hydroxide. Electron microscopy analysis showed that all phages had similar morphology, with head-tails structure, similar to those viruses of the order Caudovirales. The observed short, non-contractile tubular tails strongly indicated that phages belong to the family Autographiviridae. Phylogenetic analysis con rmed it, and revealed that the phages belong to the genus Pradovirus. The phages are closely related to each other and potentially belong a new species of the genus. These phages will be evaluated in future studies against other tomato Xanthomonads strains to assess their potential as biological control agents.

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Sheep in wolves’ clothing: Temperate T7-like bacteriophages and the origins of the Autographiviridae

Cited by 16 publications

References 76 publications

Characterization of Three Novel Virulent Aeromonas Phages Provides Insights into the Diversity of the Autographiviridae Family

Characterization of Three Novel Virulent Aeromonas Phages Provides Insights into the Diversity of the Autographiviridae Family

Transcriptomics-driven characterisation of novel T7-like temperate Pseudomonas phage LUZ100

Isolation, characterization, and evaluation of putative new bacteriophages for controlling bacterial spot on tomato in Brazil

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