Hyperexpansion of RNA Bacteriophage Diversity

Krishnamurthy, Siddharth R.; Janowski, Andrew B.; Zhao, Guoyan; Barouch, Dan H.; Wang, David

doi:10.1371/journal.pbio.1002409

Cited by 108 publications

(115 citation statements)

References 47 publications

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“…Like these factors, lys M occupies no dedicated genetic space 5 , highlighting the ability of small phages to maximize their coding capacity. Recent analysis of publicly available metagenomes and transcriptomes has revealed that the ssRNA leviviruses are more ubiquitous and diverse than previously appreciated 17,18 , at least in part because of extensive use of RNase during virome sampling. RNA phages are therefore estimated to constitute a substantial fraction of the total virome in gut samples 19 , representing a deep resource of genomic ‘dark matter’.…”

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confidence: 99%

A viral protein antibiotic inhibits lipid II flippase activity

et al. 2017

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For bacteriophage infections, the cell walls of bacteria, consisting of a single highly polymeric molecule of peptidoglycan (PG), pose a major problem for the release of progeny virions. Phage lysis proteins that overcome this barrier can point the way to new antibacterial strategies1, especially small lytic single-stranded DNA (the microviruses) and RNA phages (the leviviruses) that effect host lysis using a single non-enzymatic protein2. Previously, the A2 protein of levivirus Qβ and the E protein of the microvirus φ X174 were shown to be ‘protein antibiotics’ that inhibit the MurA and MraY steps of the PG synthesis pathway2–4. Here, we investigated the mechanism of action of an unrelated lysis protein, LysM, of the Escherichia coli levivirus M5. We show that LysM inhibits the translocation of the final lipid-linked PG precursor called lipid II across the cytoplasmic membrane by interfering with the activity of MurJ. The finding that LysM inhibits a distinct step in the PG synthesis pathway from the A2 and E proteins indicates that small phages, particularly the single-stranded RNA (ssRNA) leviviruses, have a previously unappreciated capacity for evolving novel inhibitors of PG biogenesis despite their limited coding potential.

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confidence: 99%

A viral protein antibiotic inhibits lipid II flippase activity

et al. 2017

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“…Bacteriophages (phages) are estimated to be the most abundant organisms on earth, with key roles in shaping the composition of microbial ecology by lysing bacteria or transferring genes12. Despite the numerous available studies on DNA bacteriophages, the biology of RNA bacteriophages has been poorly investigated.…”

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confidence: 99%

Characterization of the first double-stranded RNA bacteriophage infecting Pseudomonas aeruginosa

Yang

Shen

et al. 2016

Sci Rep

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Bacteriophages (phages) are widely distributed in the biosphere and play a key role in modulating microbial ecology in the soil, ocean, and humans. Although the role of DNA bacteriophages is well described, the biology of RNA bacteriophages is poorly understood. More than 1900 phage genomes are currently deposited in NCBI, but only 6 dsRNA bacteriophages and 12 ssRNA bacteriophages genome sequences are reported. The 6 dsRNA bacteriophages were isolated from legume samples or lakes with Pseudomonas syringae as the host. Here, we report the first Pseudomonas aeruginosa phage phiYY with a three-segmented dsRNA genome. phiYY was isolated from hospital sewage in China with the clinical P. aeruginosa strain, PAO38, as a host. Moreover, the dsRNA phage phiYY has a broad host range, which infects 99 out of 233 clinical P. aeruginosa strains isolated from four provinces in China. This work presented a detailed characterization of the dsRNA bacteriophage infecting P. aeruginosa.

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“…Although some phage genes are similar and functionally conserved, the number of potential genes encoded by this many phages is incomprehensible. These worldwide estimates likely even underestimate the number of phages with either single-stranded RNA or double-stranded RNA genomes, or those that dominate unique environments, as these classes may not be identified by standard phage isolation and genomic sequencing approaches (92, 93), or are under-annotated because of their divergence from more well-characterized phage (94). One of the few characterized single-stranded RNA phage is the enterobacterial phage Qβ, whose study led to the discovery of Hfq (23).…”

Section: Vast Potential To Identify New Rna Binding Proteins Regulatmentioning

confidence: 99%

Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level

2018

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The study of bacteriophages (phages) and prophages has provided key insights into almost every cellular process as well as led to the discovery of unexpected new mechanisms and the development of valuable tools. This is exemplified for RNA-based regulation. For instance, the characterization and exploitation of the anti-phage CRISPR systems is revolutionizing molecular biology. Phage-encoded proteins such as the RNA binding MS2 protein, which is broadly used to isolate tagged RNAs, also have been developed as valuable tools. Hfq, the RNA chaperone protein central to the function of many base pairing small RNAs (sRNAs), was first characterized as a bacterial host factor required for Qβ phage replication. The ongoing studies of RNAs are continuing to reveal regulatory connections between infecting phages, prophages and bacteria and to provide novel insights. There are bacterial and prophage sRNAs that regulate prophage genes, which impact bacterial virulence as well as bacterial cell killing. Conversely, phage- and prophage-encoded sRNAs modulate the expression of bacterial genes modifying metabolism. An interesting subcategory of the prophage-encoded sRNAs are sponge RNAs that inhibit the activities of bacterial-encoded sRNAs. Phages also affect post-transcriptional regulation in bacteria through proteins that inhibit or alter the activities of key bacterial proteins involved in posttranscriptional regulation. However, what is most exciting about phage and prophage research, given the millions of phage-encoded genes that have not yet been characterized, is the vast potential for discovering new RNA regulators and novel mechanisms and for gaining insight into the evolution of regulatory RNAs.

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Hyperexpansion of RNA Bacteriophage Diversity

Cited by 108 publications

References 47 publications

A viral protein antibiotic inhibits lipid II flippase activity

A viral protein antibiotic inhibits lipid II flippase activity

Characterization of the first double-stranded RNA bacteriophage infecting Pseudomonas aeruginosa

Cross-Regulation between Bacteria and Phages at a Posttranscriptional Level

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