Mycobacteriophage Marvin: a New Singleton Phage with an Unusual Genome Organization

Abstract

bMycobacteriophages represent a genetically diverse group of viruses that infect mycobacterial hosts. Although more than 80 genomes have been sequenced, these still poorly represent the likely diversity of the broader population of phages that can infect the host, Mycobacterium smegmatis mc 2 155. We describe here a newly discovered phage, Marvin, which is a singleton phage, having no previously identified close relatives. The 65,100-bp genome contains 107 predicted protein-coding genes arranged in a noncanonical genomic architecture in which a subset of the minor tail protein genes are displaced about 20 kbp from their typical location, situated among nonstructural genes anticipated to be expressed early in lytic growth. Marvin is not temperate, and stable lysogens cannot be recovered from infections, although the presence of a putative xis gene suggests that Marvin could be a relatively recent derivative of a temperate parent. The Marvin genome is replete with novel genes not present in other mycobacteriophage genomes, and although most are of unknown function, the presence of amidoligase and glutamine amidotransferase genes suggests intriguing possibilities for the interactions of Marvin with its mycobacterial hosts.

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

“…Rey gp35 is glycine rich (Ͼ16%)-a not uncommon feature of phage tail fiber proteins-and is more closely related to cluster L tail proteins (e.g., LeBron gp21; 27% amino acid identity) than to the cluster M1 phages. The minor tail protein gene cluster extends through to Bongo gene 34, PegLeg gene 34, and Rey gene 39, and the last of these is related to the gene for Marvin gp57, which has been shown to be a virion component (16). In addition, Rey gp39 was identified as a virion component by mass spectrometry (see below; Table 2).…”

“…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). Cluster A phages have a complex immunity system in which the repressor binds to multiple stoperator sites located throughout the genome (14,17), and in the cluster G phages, establishment of immunity is unusually dependent on phage integration (18).…”

The First Structure of a Mycobacteriophage, the Mycobacterium abscessus subsp. bolletii Phage Araucaria

“…3). This ϳ25-kb segment is among the smallest virion structure and assembly cassettes observed in mycobacteriophages, along with those from mycobacteriophage BP (24 kb) and mycobacteriophage Marvin (20 kb) (33,34). A putative function was assigned to the ORF55, -57, and -62 proteins on the basis of their similarity to proteins of mycobacteriophage Dori and members of cluster B.…”

Mycobacteriophages

“…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). …”