Chapter 5 - Genomics of Staphylococcal Twort-like Phages - Potential Therapeutics of the Post-Antibiotic Era
Introduction
The Staphylococcus genus groups several species of Gram-positive bacteria that inhabit human or animal organisms. Many of these species, especially Staphylococcus aureus, include highly pathogenic strains that can cause infections, which are manifested by various symptoms ranging from relatively mild to life threatening (reviewed by Tenover and Gorwitz, 2006). The treatment of such infections is becoming increasingly problematic due to the dissemination of methicillin-resistant S. aureus, as well as the emergence of vancomycin-resistant strains (Arias and Murray, 2009, Chambers and DeLeo, 2009, Howden et al., 2010). Naturally occurring, virulent bacteriophages that infect and kill a wide range of staphylococcal strains may become an alternative in the treatment of otherwise incurable infections caused by antibiotic-resistant staphylococci (Borysowski, 2011, Mann, 2008, Merabishvili et al., 2009). A few of them were shown to be effective in the treatment of staphylococcal infections in animals or are used in phage therapy including clinical trials in humans (Capparelli et al., 2007, Gill et al., 2006; Gupta and Prasad, 2011, Jikia et al., 2005, Kvachadze et al., 2011, Markoishvili et al., 2002, Merabishvili et al., 2009, Paul et al., 2011a; O'Flaherty et al., 2005b, Rhoads et al., 2009; Sulakvelidze et al., 2001; Sulakvelidze and Kutter, 2005, Sunagar et al., 2010, Wills et al., 2005; Zimecki et al., 2008, Zimecki et al., 2009, Zimecki et al., 2010). Additionally, proteins of these phages that are lethal to Staphylococci may serve as prototypes of antibacterials, mark potential drug targets in staphylococcal cells, or can be used as anti-staphylococcal agents by themselves (Fischetti, 2008, Gu et al., 2011; Liu et al., 2004, Pastagia et al., 2011, Projan, 2004; Rashel et al., 2007). Phages of the most promising group from a therapeutic point of view belong to the Twort-like genus (Klumpp et al., 2010). Although their history dates as far back as the history of phages, with their first representative, phage Twort, believed to have been isolated in 1915 (Lavigne et al., 2009, Twort, 1915), little is yet known about the biology of these phages. This chapter provides the genome-wide comparison of 11 staphylococcal Twort-like phages, which are suitable for therapeutic applications. Some genomic features of these phages which appear to be responsible for their certain properties and wide strain specificity are also discussed.
Section snippets
Staphylococcal Bacteriophages: A Short Overview
Early interest in staphylococcal phages was stimulated by their potential therapeutic applications (reviewed by Alisky et al., 1998, Sulakvelidze and Kutter, 2005; Sulakvelidze et al., 2001). However, after the introduction of antibiotics, it was motivated mainly by the wide application of phages to differentiate clinical staphylococcal strains. The method of phage typing of staphylococci derived from this early work and originally developed by Wilson and Atkinson (1945) has been used,
Morphology
Morphologically, staphylococcal Twort-like phages resemble phages of the same genus that infect Listeria monocytogenes (A511, P100) and differ from Bacillus phage SPO1 by having longer tails (from 175–176 nm in ISP and 676Ż to 217–219 nm in K and P4W/Fi200W versus 140 nm in SPO1), which are also slightly more slender (Fig. 1; Duda et al., 2006, Hotchin, 1954, Jarvis et al., 1993; Klumpp et al., 2008, 2010, and references therein; Kwiatek et al., 2012; Ulatowska et al., in preparation). However,
Concluding Remarks
Genomic characterization of large obligatorily virulent bacteriophages on a mass scale became possible only recently with the advent of high-throughput cloning-independent sequencing technologies. The comparison of 11 phage genomic sequences presented in this chapter is only a small step toward understanding the biology of staphylococcal Twort-like phages and the biology of the Spounavirinae subfamily of myoviruses they belong to. Functional analysis of knockout mutants in genes of undetermined
Acknowledgments
The authors are grateful to Hans-Wolfgang Ackermann for help in the description of phage morphological features and to Wacław Szybalski for helpful comments on this manuscript. This work was supported by funds from the Operational Program ‘Innovative Economy, 2007-2013’ (Priority axis 1. Research and Development of Modern Technologies, Measure 1.3 Support for R&D projects for entrepreneurs carried out by scientific entities, Submeasure 1.3.1, Development Project No. POIG 01.03.01-02-003/08
References (273)
Tailed bacteriophages: The order caudovirales
Adv. Virus Res.
(1998)- et al.
Curated list of prokaryote viruses with fully sequenced genomes
Res. Microbiol.
(2007) - et al.
Bacteriophages show promise as antimicrobial agents
J. Infect.
(1998) - et al.
Role of RNA in bacteriophage phi 29 DNA packaging
J. Struct. Biol.
(1990) - et al.
Failure of bacteriophage typing to detect an inter-hospital outbreak of methicillin-resistant Staphylococcus aureus (MRSA) in Zagreb subsequently identified by random amplification of polymorphic DNA (RAPD) and pulsed-field gel electrophoresis (PFGE)
Clin. Microbiol. Infect.
(1999) - et al.
Genome and virulence determinants of high virulence community-acquired MRSA
Lancet
(2002) - et al.
Structure, assembly, and DNA packaging of the bacteriophage T4 head
Adv. Virus Res.
(2012) - et al.
Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved
Trends Microbiol.
(2002) - et al.
Bacteriophage P100 for control of Listeria monocytogenes in foods: Genome sequence, bioinformatic analyses, oral toxicity study, and application
Regul. Toxicol. Pharmacol.
(2005) - et al.
Serotype F double- and triple-converting phage insertionally inactivate the Staphylococcus aureus beta-toxin determinant by a common molecular mechanism
FEMS Microbiol. Lett.
(1993)
Interaction of Bacillus subtilis RNA polymerase core with two specificity-determining subunits: Competition between sigma and the SPO1 gene 28 protein
J. Biol. Chem.
The complete genomes of Staphylococcus aureus bacteriophages 80 and 80α–implications for the specificity of SaPI mobilization
Virology
Modular architecture of the T4 phage superfamily: a conserved core genome and a plastic periphery
Virology.
Overproduction and purification of a bacteriophage SPO1-encoded RNA polymerase sigma factor
J. Biol. Chem.
Characterization of the primary sigma factor of Staphylococcus aureus
J. Biol. Chem.
Shared architecture of bacteriophage SPO1 and herpesvirus capsids
Curr. Biol.
Bacteriophage lysins as effective antibacterials
Curr. Opin. Microbiol.
Immunoglobulin-like domains on bacteriophage: Weapons of modest damage?
Curr. Opin. Microbiol.
Ig-like domains on bacteriophages: A tale of promiscuity and deceit
J. Mol. Biol.
Transcription during bacteriophage SPO1 development: Mutations affecting the program of viral transcription
J. Mol. Biol.
Isolation and characterization of BsuE methyltransferase, a CGCG specific DNA methyltransferase from Bacillus subtilis
J. Biol. Chem.
TF1, a bacteriophage-specific DNA-binding and DNA bending protein
J. Struct. Biol.
A reliable method for storage of tailed phages
J. Microbiol. Methods.
Comparative analysis of the genomes of the temperate bacteriophages phi 11, phi 12 and phi 13 of Staphylococcus aureus 8325
Gene
Two DNA antirestriction systems of bacteriophage P1, darA, and darB: Characterization of darA- phages
Virology
Basic phage electron microscopy
Methods Mol. Biol.
Viruses of Prokaryotes II: Natural Groups of Bacteriophages
5500 Phages examined in the electron microscope
Arch. Virol.
A new approach to establishing the set of phages for typing methicillin-resistant Staphylococcus aureus
J. Chemother.
The phage ϕ29 membrane protein p16.7, involved in DNA replication, is required for efficient ejection of the viral genome
J. Bacteriol.
Bacteriophage typing of enteric pathogens and staphylococci and its use in epidemiology
J. Clin. Pathol.
Blocking of bacteriophage receptor sites by Concanavalin A
J. Gen. Microbiol.
Antibiotic-resistant bugs in the 21st century - a clinical super-challenge
N. Engl. J. Med.
Characterisation of the structure of ocr, the gene 0.3 protein of bacteriophage T7
Nucleic Acids Res
Reaction difference rule for phage typing of Staphylococcus aureus at 100 times the routine test dilution
J. Clin. Microbiol.
Preliminary analysis of the genetic basis for vancomycin resistance in Staphylococcus aureus strain Mu50
J. Antimicrob. Chemother.
Prophages of Staphylococcus aureus Newman and their contribution to virulence
Mol. Microbiol.
LysK CHAP endopeptidase domain is required for lysis of live staphylococcal cells
FEMS Microbiol. Lett.
The thioredoxin binding domain of bacteriophage T7 DNA polymerase confers processivity on Escherichia coli DNA polymerase I
Proc. Natl. Acad. Sci. USA.
Competition of bacteriophage polypeptides with native replicase proteins for binding to the DNA sliding clamp reveals a novel mechanism for DNA replication arrest in Staphylococcus aureus
Mol. Microbiol.
Staphylococcal enterotoxin A is encoded by phage
Science
Morphogenesis of bacteriophage phi 29 of Bacillus subtilis: DNA-gp3 intermediate in in vivo and in vitro assembly
J. Virol.
Phage typing of staphylococci
Bull. WHO
Potential of bacteriophages and their lysins in the treatment of MRSA: current status and future perspectives
BioDrugs
Stability analysis of the bacteriophage phiKMV lysin gp36C and its putative role during infection
Cell Mol. Life Sci.
Phages and the evolution of bacterial pathogens: From genomic rearrangements to lysogenic conversion
Microbiol. Mol. Biol. Rev.
Comparative phage genomics and the evolution of Siphoviridae: Insights from dairy phages
Mol. Microbiol.
Temporal expression of adhesion factors and activity of global regulators during establishment of Staphylococcus aureus nasal colonization
J. Infect. Dis.
Experimental phage therapy against Staphylococcus aureus in mice
Antimicrob. Agents. Chemother.
Determining DNA packaging strategy by analysis of the termini of the chromosomes in tailed-bacteriophage virions
Methods Mol. Biol.
Cited by (94)
Characterizations of the endolysin Lys84 and its domains from phage qdsa002 with high activities against Staphylococcus aureus and its biofilms
2021, Enzyme and Microbial TechnologyCitation Excerpt :Therefore, phage qdsa002 can be assigned to Twort-like phage based on the above analysis. It was reported that Twort-like phages can fast and efficiently adsorb to the host cells and have the short latent period as well as the strong biofilm penetration ability [25,26]. The phages that infect S. aureus from this group and their endolysins are the most promising candidates for therapeutic applications in S. aureus and the bacterial biofilms [27,28].
The lytic bacteriophage vB_EfaH_EF1TV, a new member of the Herelleviridae family, disrupts biofilm produced by Enterococcus faecalis clinical strains
2020, Journal of Global Antimicrobial ResistanceDiscovery of the First Lytic Staphylococcus pseudintermedius/Staphylococcus aureus Polyvalent Bacteriophages
2022, PHAGE: Therapy, Applications, and Research