Cluster J Mycobacteriophages: Intron Splicing in Capsid and Tail Genes

Pope, Welkin H.; Jacobs-Sera, Deborah; Best, Aaron A.; Broussard, Gregory W.; Connerly, Pamela L.; Dedrick, Rebekah M.; Kremer, Timothy; Offner, Susan; Ogiefo, Amenawon H.; Pizzorno, Marie C.; Rockenbach, Kate; Russell, Daniel A.; Stowe, Emily L.; Stukey, Joseph; Thibault, Sarah A.; Conway, James F.; Hendrix, Roger W.; Hatfull, Graham F.

doi:10.1371/journal.pone.0069273

Cited by 29 publications

(50 citation statements)

References 50 publications

(75 reference statements)

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“…The 285 mycobacteriophage genomes currently available in GenBank are all dsDNA tailed phages classified morphologically as either siphoviral or myoviral and encompass substantial sequence diversity (4)(5)(6). Comparison at the nucleotide sequence level reveals groups of genomes that are more closely related to each other than to others, and these are referred to as clusters; members of a cluster typically share nucleotide sequence similarity that spans more than 50% of their genome lengths and have closely related gene contents (7).…”

Section: Mycobacteriophages-viruses Of Mycobacterial Hosts Such Asmentioning

confidence: 99%

“…In the phages with siphoviral morphologies (all phages except those of cluster C), the 25 to 30 virion structure and assembly genes have a shared synteny. The genes either can be tightly packed and occupy minimal genome space (e.g., 23 kbp in cluster G phages [15]) or can be interspersed with apparently nonstructure genes expanding the operon to over 35 kbp (e.g., cluster J [5]). In phage Marvin, several of the tail genes are displaced and relocated about 20 kbp from their canonical position (16).…”

Section: Mycobacteriophages-viruses Of Mycobacterial Hosts Such Asmentioning

confidence: 99%

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Cluster M Mycobacteriophages Bongo, PegLeg, and Rey with Unusually Large Repertoires of tRNA Isotypes

Pope

Anders

Baird

et al. 2014

J Virol

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Genomic analysis of a large set of phages infecting the common host Mycobacterium smegmatis mc 2 155 shows that they span considerable genetic diversity. There are more than 20 distinct types that lack nucleotide similarity with each other, and there is considerable diversity within most of the groups. Three newly isolated temperate mycobacteriophages, Bongo, PegLeg, and Rey, constitute a new group (cluster M), with the closely related phages Bongo and PegLeg forming subcluster M1 and the more distantly related Rey forming subcluster M2. The cluster M mycobacteriophages have siphoviral morphologies with unusually long tails, are homoimmune, and have larger than average genomes (80.2 to 83.7 kbp). They exhibit a variety of features not previously described in other mycobacteriophages, including noncanonical genome architectures and several unusual sets of conserved repeated sequences suggesting novel regulatory systems for both transcription and translation. In addition to containing transfer-messenger RNA and RtcB-like RNA ligase genes, their genomes encode 21 to 24 tRNA genes encompassing complete or nearly complete sets of isotypes. We predict that these tRNAs are used in late lytic growth, likely compensating for the degradation or inadequacy of host tRNAs. They may represent a complete set of tRNAs necessary for late lytic growth, especially when taken together with the apparent lack of codons in the same late genes that correspond to tRNAs that the genomes of the phages do not obviously encode. IMPORTANCEThe bacteriophage population is vast, dynamic, and old and plays a central role in bacterial pathogenicity. We know surprisingly little about the genetic diversity of the phage population, although metagenomic and phage genome sequencing indicates that it is great. Probing the depth of genetic diversity of phages of a common host, Mycobacterium smegmatis, provides a higher resolution of the phage population and how it has evolved. Three new phages constituting a new cluster M further expand the diversity of the mycobacteriophages and introduce novel features. As such, they provide insights into phage genome architecture, virion structure, and gene regulation at the transcriptional and translational levels.T he bacteriophage population is large, dynamic, old, and genetically diverse (1). Over 1,000 phage genomes have been sequenced, and the majority are double-stranded DNA (dsDNA) tailed phages, classified morphologically in the order Caudovirales. The genomes of dsDNA tailed phages vary in length from ϳ20 kbp to over 500 kbp (2) and typically contain 20 to 30 genes encoding virion structure and assembly functions, genes coding for DNA and nucleotide metabolism, a lysis cassette, and regulatory systems. The genomes of temperate phages typically encode repressors, contain operators, and frequently include systems for phage genome integration. However, with the exception of the few well-studied phage prototypes, the majority of genes carried by phages are of unknown function (1). Mycobacteriophages-vir...

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Section: Mycobacteriophages-viruses Of Mycobacterial Hosts Such Asmentioning

confidence: 99%

Section: Mycobacteriophages-viruses Of Mycobacterial Hosts Such Asmentioning

confidence: 99%

Cluster M Mycobacteriophages Bongo, PegLeg, and Rey with Unusually Large Repertoires of tRNA Isotypes

Pope

Anders

Baird

et al. 2014

J Virol

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“…In other genomes, the gene order may be conserved, but the virion structure and assembly genes are interspersed with non-structural genes. In phage Omega and its relatives (52), the virion structure and assembly genes span over 35kbp, and the inserted genes include a glycosyl transferase, an O-methyl transferase, and an IS110-like transposon. In phage Marvin and its relatives two of the minor tail protein genes are atypically located near the right end of the genome, separated by about 20 kbp from the other structural genes (53).…”

Section: Mycobacteriophage Genome Organization and Expressionmentioning

confidence: 99%

“…There is an IS 110 -like element in phage Omega and some other Cluster J phages (52), IS 605 -like elements in phage Llij and several other Subcluster F1 phages – although inserted at several distinct locations – an IS 1096 -like element in the Cluster G phage LouisV14, and an IS 1380 -like element in Guillsminger (Subcluster K5). There are instances of introns (e.g.…”

Section: Insights Into Phage Evolutionmentioning

confidence: 99%

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Mycobacteriophages

Hatfull

2018

Microbiol Spectr

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Mycobacteriophages are viruses that infect mycobacterial hosts. A large number of mycobacteriophages have been isolated and genomically characterized, providing insights into viral diversity and evolution, as well as fueling development of tools for mycobacterial genetics. Mycobacteriophages have intimate relationships with their hosts, and provide insights into the genetics and physiology of the mycobacteria, and tools for potential clinical applications such as drug development, diagnosis, vaccines, and potentially therapy.

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A Parallel Adder Coordinates Mycobacterial Cell-Cycle Progression and Cell-Size Homeostasis in the Context of Asymmetric Growth and Organization

et al. 2017

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Summary In model bacteria, such as E. coli and B. subtilis, regulation of cell cycle progression and cellular organization achieves consistency in cell size, replication dynamics, and chromosome positioning [1–3]. Mycobacteria elongate and divide asymmetrically, giving rise to significant variation in cell size and elongation rate among closely related cells [4, 5]. Given the physical asymmetry of mycobacteria, the models that describe coordination of cellular organization and cell cycle progression in model bacteria are not directly translatable [1, 2, 6–8]. Here we used time-lapse microscopy and fluorescent reporters of DNA replication and chromosome positioning to examine the coordination of growth, division, and chromosome dynamics at a single-cell level in Mycobacterium smegmatis (M. smegmatis) and Mycobacterium bovis Bacillus Calmette–Guérin (BCG). By analyzing chromosome and replisome localization, we demonstrated that chromosome positioning is asymmetric and proportional to cell size. Furthermore, we found that cellular asymmetry is maintained throughout the cell cycle and is not established at division. Using measurements and stochastic modeling of mycobacterial cell size and cycle timing in both slow and fast growth conditions, we found that well-studied cell size control models are insufficient to explain the mycobacterial cell cycle. Instead, we showed that mycobacterial cell cycle progression is regulated by an unprecedented mechanism involving parallel adders (i.e. constant growth increments) that start at replication initiation. Together, these adders enable mycobacterial populations to regulate cell size, growth, and heterogeneity in the face of varying environments.

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Cluster J Mycobacteriophages: Intron Splicing in Capsid and Tail Genes

Cited by 29 publications

References 50 publications

Cluster M Mycobacteriophages Bongo, PegLeg, and Rey with Unusually Large Repertoires of tRNA Isotypes

Cluster M Mycobacteriophages Bongo, PegLeg, and Rey with Unusually Large Repertoires of tRNA Isotypes

Mycobacteriophages

A Parallel Adder Coordinates Mycobacterial Cell-Cycle Progression and Cell-Size Homeostasis in the Context of Asymmetric Growth and Organization

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