Analysis of some phenotypic traits of feces-borne temperate lambdoid bacteriophages from different immunity groups: a high incidence of cor+, FhuA-dependent phages

Hernández‐Sánchez, Javier; Bautista-Santos, Arnulfo; Fernández, Luis; Bermúdez‐Cruz, Rosa María; Uc-Mass, Augusto; Martínez-Peñafiel, Eva; Martínez, Mario A.; García‐Mena, Jaime; Guarneros, Gabriel; Kameyama, Luis

doi:10.1007/s00705-008-0111-0

Cited by 10 publications

(6 citation statements)

References 54 publications

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“…Lipoproteins (encoded by the cor genes) are found in a number of phages, in which they prevent superinfection by inactivating the receptors. For example, a protein product of the N15 gene 24 , the homolog and functional analog of the Cor phage ϕ80 [ 48 ] is responsible for the inability of N15 lysogens to adsorb FhuA-dependent bacteriophages N15, T1, and ϕ80 [ 49 – 51 ]. The cor genes of N15, ϕ80 and Rtp phages are located next to the tail fiber genes [ 49 ].…”

Section: Resultsmentioning

confidence: 99%

Two Inducible Prophages of an Antarctic Pseudomonas sp. ANT_H14 Use the Same Capsid for Packaging Their Genomes – Characterization of a Novel Phage Helper-Satellite System

Dziewit

Radlińska

2016

PLoS ONE

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Two novel prophages ФAH14a and ФAH14b of a psychrotolerant Antarctic bacterium Pseudomonas sp. ANT_H14 have been characterized. They were simultaneously induced with mitomycin C and packed into capsids of the same size and protein composition. The genome sequences of ФAH14a and ФAH14b have been determined. ФAH14b, the phage with a smaller genome (16,812 bp) seems to parasitize ФAH14a (55,060 bp) and utilizes its capsids, as only the latter encodes a complete set of structural proteins. Both viruses probably constitute a phage helper-satellite system, analogous to the P2-P4 duo. This study describes the architecture and function of the ФAH14a and ФAH14b genomes. Moreover, a functional analysis of a ФAH14a-encoded lytic enzyme and a DNA methyltransferase was performed. In silico analysis revealed the presence of the homologs of ФAH14a and ФAH14b in other Pseudomonas genomes, which may suggest that helper-satellite systems related to the one described in this work are common in pseudomonads.

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Section: Resultsmentioning

confidence: 99%

Two Inducible Prophages of an Antarctic Pseudomonas sp. ANT_H14 Use the Same Capsid for Packaging Their Genomes – Characterization of a Novel Phage Helper-Satellite System

Dziewit

Radlińska

2016

PLoS ONE

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“…For example, the Cor protein from the 80 prophage inactivates the cell surface receptor FhuA (37), resulting in the inability of 80 itself to infect the host. Other phages that require this receptor (e.g., phages T1, T5, HK022, and N15), as well as toxins that are imported through it (e.g., colicin M), are likewise unable to infect cells that express the Cor protein (13,15). Other proteins expressed from morons, such as Salmonella phage P22 SieA (33), E. coli phage T4 Sp and Imm (25,26), and Lactococcus lactis phage Tuc2009 Sie 2009 (27), prevent entry of phage DNA at a point downstream of the initial receptor binding event.…”

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confidence: 99%

The Bacteriophage HK97 gp15 Moron Element Encodes a Novel Superinfection Exclusion Protein

et al. 2012

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ABSTRACTA phage moron is a DNA element inserted between a pair of genes in one phage genome that are adjacent in other related phage genomes. Phage morons are commonly found within phage genomes, and in a number of cases, they have been shown to mediate phenotypic changes in the bacterial host. The temperate phage HK97 encodes a moron element, gp15, within its tail morphogenesis region that is absent in most closely related phages. We show that gp15 is actively expressed from the HK97 prophage and is responsible for providing the host cell with resistance to infection by phages HK97 and HK75, independent of repressor immunity. To identify the target(s) of this gp15-mediated resistance, we created a hybrid of HK97 and the related phage HK022. This hybrid phage revealed that the tail tube or tape measure proteins likely mediate the susceptibility of HK97 to inhibition by gp15. The N terminus of gp15 is predicted with high probability to contain a single membrane-spanning helix by several transmembrane prediction programs. Consistent with this putative membrane localization, gp15 acts to prevent the entry of phage DNA into the cytoplasm, acting in a manner reminiscent of those of several previously characterized superinfection exclusion proteins. The N terminus of gp15 and its phage homologues bear sequence similarity to YebO proteins, a family of proteins of unknown function found ubiquitously in enterobacteria. The divergence of their C termini suggests that phages have co-opted this bacterial protein and subverted its activity to their advantage.

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“…A clear plaque mutant of phage mEp043 was used for DNA extraction because its lysate yielded a higher titer. All other phages are likely to be identical to those described in earlier publications (38)(39)(40). Phages with the prefix HK were isolated by Elvera and Tarlochan Dhillon in the 1970s and early 1980s from different sources in Hong Kong (some of which are referenced in (41)) and were provided to us by Rodney King (Western Kentucky University, KY).…”

Section: Datamentioning

confidence: 86%

Co-transfer of functionally interdependent genes contributes to genome mosaicism in lambdoid phages

Kupczok

Bailey

Refardt

et al. 2022

Preprint

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Lambdoid (or Lambda-like) phages, are a group of related temperate phages that can infect Escherichia coli and other gut bacteria. A key characteristic of these phages is their mosaic genome structure which served as basis for the “modular genome hypothesis”. Accordingly, lambdoid phages evolve by transferring genomic regions, each of which constitutes a functional unit. Nevertheless, it is unknown which genes are preferentially transferred together and what drives such co-transfer events. Here we aim to characterize genome modularity by studying co-transfer of genes among 95 distantly related lambdoid (pro-)phages. Based on gene content, we observed that the genomes cluster into twelve groups, which are characterized by a highly similar gene content within the groups and highly divergent gene content across groups. Highly similar proteins can occur in genomes of different groups, indicating that they have been transferred. About 26% of homologous protein clusters in the four known operons (i.e., the early left, early right, immunity, and late operon) engage in gene transfer, which affects all operons to a similar extent. We identified pairs of genes that are frequently co-transferred and observed that these pairs tend to be in close proximity to one another on the genome. We find that frequently co-transferred genes are involved in related functions and highlight interesting examples involving structural proteins, the CI repressor and Cro regulator, proteins interacting with DNA, and membrane-interacting proteins. We conclude that epistatic effects, where the functioning of one protein depends on the presence of another, plays an important role in the evolution of the modular structure of these genomes.Data summaryThe genomes used in this research are publicly available (Table S1). All supporting data is available in supplementary tables. Source code and documentation to calculate GRR is available under GPLv2 (https://github.com/annecmg/GRRpair).Impact statementTemperate phages, viruses that can integrate their own genetic material into bacterial genomes, are pervasive mobile genetic elements that can influence bacterial fitness in manifold ways. The E. coli phage lambda has been a model phage of molecular biology for decades. Lambdoid phages are highly prevalent in Enterobacteria such as E. coli and Salmonella, have a mosaic-like genome, the same genome architecture as lambda, and can recombine with phage lambda. Nevertheless, these phages can be very distinct, and no lambdoid core genome exits. Although lambdoid phage genomes have been studied for decades, we know relatively little about how they evolve. Early observations led to the modular genome hypothesis, according to which, phages are assemblages of genetic modules. But what determines the structure of these modules and which genes do preferentially occur together in modules? In this study, we provide answers to these questions using a novel computational approach that allows to infer gene transfer events between distantly related phages despite the absence of a core genome.We find that co-transfer of functionally related genes is frequent during the evolution of lambdoid phages. This suggests epistatic interactions among these genes, i.e., the co-transferred genes likely need to function together to ensure a viable phage. A prime example is the co-transfer of structural genes, such as genes encoding for the phage capsid or the phage tail. Additionally, we also find co-transfer of known interacting regulatory genes and co-transfer between functionally related genes that have so far been unknown to interact. Together, our analysis provides novel insights into the evolution of temperate phages. Moreover, our approach, which allows to identify gene transfer in the absence of a core phylogeny might be valuable for studying the evolution of other fast-evolving genomes, including viruses of other hosts.

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Analysis of some phenotypic traits of feces-borne temperate lambdoid bacteriophages from different immunity groups: a high incidence of cor+, FhuA-dependent phages

Cited by 10 publications

References 54 publications

Two Inducible Prophages of an Antarctic Pseudomonas sp. ANT_H14 Use the Same Capsid for Packaging Their Genomes – Characterization of a Novel Phage Helper-Satellite System

Two Inducible Prophages of an Antarctic Pseudomonas sp. ANT_H14 Use the Same Capsid for Packaging Their Genomes – Characterization of a Novel Phage Helper-Satellite System

The Bacteriophage HK97 gp15 Moron Element Encodes a Novel Superinfection Exclusion Protein

Co-transfer of functionally interdependent genes contributes to genome mosaicism in lambdoid phages

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