On the nature of mycobacteriophage diversity and host preference

Jacobs-Sera, Deborah; Marinelli, Laura J.; Bowman, Charles A.; Broussard, Gregory W.; Bustamante, Carlos A. Guerrero; Boyle, Michelle M.; Petrova, Zaritza O.; Dedrick, Rebekah M.; Pope, Welkin H.; Modlin, Robert L.; Hendrix, Roger W.; Hatfull, Graham F.

doi:10.1016/j.virol.2012.09.026

Cited by 165 publications

(202 citation statements)

References 70 publications

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“…The third protein is Basilisk's tail fiber protein (gp51), which is one of only two proteins also encoded by JL and Shanette (38% identity). Since all three phages display the same host range (Table 1), these results are consistent with tail fibers being a highly recombinogenic host determinant (63,64). The tail fiber has homology to carbohydrate binding proteins (CenC from B. cereus is 43% identical over 103 amino acids), which suggests that carbohydrates are involved in host recognition.…”

Section: Figsupporting

confidence: 70%

The Genomes, Proteomes, and Structures of Three Novel Phages That Infect the Bacillus cereus Group and Carry Putative Virulence Factors

Grose

Belnap

Jensen

et al. 2014

J Virol

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This article reports the results of studying three novel bacteriophages, JL, Shanette, and Basilisk, which infect the pathogen Bacillus cereus and carry genes that may contribute to its pathogenesis. We analyzed host range and superinfection ability, mapped their genomes, and characterized phage structure by mass spectrometry and transmission electron microscopy (TEM). The JL and Shanette genomes were 96% similar and contained 217 open reading frames (ORFs) and 220 ORFs, respectively, while Basilisk has an unrelated genome containing 138 ORFs. Mass spectrometry revealed 23 phage particle proteins for JL and 15 for Basilisk, while only 11 and 4, respectively, were predicted to be present by sequence analysis. Structural protein homology to wellcharacterized phages suggested that JL and Shanette were members of the family Myoviridae, which was confirmed by TEM. The third phage, Basilisk, was similar only to uncharacterized phages and is an unrelated siphovirus. Cryogenic electron microscopy of this novel phage revealed a T‫9؍‬ icosahedral capsid structure with the major capsid protein (MCP) likely having the same fold as bacteriophage HK97 MCP despite the lack of sequence similarity. Several putative virulence factors were encoded by these phage genomes, including TerC and TerD involved in tellurium resistance. Host range analysis of all three phages supports genetic transfer of such factors within the B. cereus group, including B. cereus, B. anthracis, and B. thuringiensis. This study provides a basis for understanding these three phages and other related phages as well as their contributions to the pathogenicity of B. cereus group bacteria. IMPORTANCEThe Bacillus cereus group of bacteria contains several human and plant pathogens, including B. cereus, B. anthracis, and B. thuringiensis. Phages are intimately linked to the evolution of their bacterial hosts and often provide virulence factors, making the study of B. cereus phages important to understanding the evolution of pathogenic strains. Herein we provide the results of detailed study of three novel B. cereus phages, two highly related myoviruses (JL and Shanette) and an unrelated siphovirus (Basilisk). The detailed characterization of host range and superinfection, together with results of genomic, proteomic, and structural analyses, reveal several putative virulence factors as well as the ability of these phages to infect different pathogenic species.

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Section: Figsupporting

confidence: 70%

The Genomes, Proteomes, and Structures of Three Novel Phages That Infect the Bacillus cereus Group and Carry Putative Virulence Factors

Grose

Belnap

Jensen

et al. 2014

J Virol

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“…The cluster M phages thus represent an interesting new group displaying a variety of novel features. We have suggested previously that the broad span of mycobacteriophage diversity and their broad range of GC contents reflects an evolutionary history in which phages migrate rapidly across a landscape of closely related but diverse bacterial hosts at relatively high frequencies (20). The cluster M phages may thus have accessed M. smegmatis mc 2 155 as a host in their recent evolutionary past but took a distinct evolutionary path, accessing a spectrum of hosts that differs from that of mycobacteriophage clusters.…”

Section: Discussionmentioning

confidence: 99%

“…The origins of all this diversity are not clear, but it has been suggested that it reflects the ability of the viruses to relatively rapidly switch from one host to another. This ability then enables a speedy migration across the bacterial landscape, provided that a diverse set of relatively closely related bacterial cells is present in that environment (20). Viral genomes are architecturally mosaic, and gene acquisition by horizontal exchange provides a mechanism for rapid adaptation to new host environments (13,20,21).…”

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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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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“…These variations might be associated with the ability to expand their host range as observed for L5-like viruses (24). Also, keeping in mind that the number of protein encoding genes is constant for members of a particular virus species, the differential distribution of SSRs introduces variable potential in the genomes to evolve through copy number and sequence alterations.…”

Section: Prevalence Of Ssr and Cssrmentioning

confidence: 99%

Microsatellite Diversity and Complexity in Eighteen Staphylococcus Phage Genomes

Alam

Iqbal²,

Tripathi

et al. 2017

Gene Cell Tissue

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The present study focused on Staphylococcus phage genomes, which have been classified to 3 categories on the basis of their size. Overall, 18 classes of II Staphylococcus phage genomes with genome size around 40 kbp were investigated to elucidate the presence, distribution, and complexity of SSRs therein. The full length genome sequences from NCBI were analyzed using the IMEx software. A total of 3656 simple sequence repeats (SSRs) and 213 compound SSRs (cSSR) were present in the studied genomes. The incident frequency of SSR and cSSR per genome ranged from 183 to 308 and 8 to 19, respectively. The SSRs distribution across genomes was non-linear and so was its conversion to cSSR (the range of cSSR percentage was from 4.15 to 9.13) implicating a non-uniform incidence and clustering in genomes. The AT rich content of genomes was reflected in the prevalence of repeats with A, AT/TA, and AAG/GAA being the highest represented mono-, di-, and tri-nucleotide repeat motifs, respectively. An increase in dMAX was accompanied by greater cSSRs in the genomes yet the increase was neither uniform across genomes nor linear. The SSRs and cSSRs are predominantly localized on the coding region. The non-coding region accounts for~19% in SSR and~30% in cSSR while a hypothetical protein accounted for~30% in SSRs as well as cSSR. The relative frequencies and distribution of different classes of simple and compound microsatellites within and across genomes are suggestive of these sequences being involved in genome evolution and adaptation.

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On the nature of mycobacteriophage diversity and host preference

Cited by 165 publications

References 70 publications

The Genomes, Proteomes, and Structures of Three Novel Phages That Infect the Bacillus cereus Group and Carry Putative Virulence Factors

The Genomes, Proteomes, and Structures of Three Novel Phages That Infect the Bacillus cereus Group and Carry Putative Virulence Factors

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

Microsatellite Diversity and Complexity in Eighteen Staphylococcus Phage Genomes

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