Bacteriophage resistance mechanisms

Phages are now acknowledged as the most abundant microorganisms on the planet and are also possibly the most diversified. This diversity is mostly driven by their dynamic adaptation when facing selective pressure such as phage resistance mechanisms, which are widespread in bacterial hosts. When infecting bacterial cells, phages face a range of antiviral mechanisms, and they have evolved multiple tactics to avoid, circumvent or subvert these mechanisms in order to thrive in most environments. In this Review, we highlight the most important antiviral mechanisms of bacteria as well as the counter-attacks used by phages to evade these systems.

[1]  G. Vovis,et al.  Complementary action of restriction enzymes endo R-DpnI and Endo R-DpnII on bacteriophage f1 DNA. , 1977, Journal of molecular biology.

[2]  D. Mcclean The capsulation of streptococci and its relation to diffusion factor (hyaluronidase) , 1941 .

[3]  T. Bickle,et al.  Bacteriophage survival: multiple mechanisms for avoiding the deoxyribonucleic acid restriction systems of their hosts. , 1983, Microbiological reviews.

[4]  John H. White,et al.  The structure of M.EcoKI Type I DNA methyltransferase with a DNA mimic antirestriction protein , 2008, Nucleic acids research.

[5]  K. Tait,et al.  The interaction of phage and biofilms. , 2004, FEMS microbiology letters.

[6]  R. Hutkins Microbiology and Technology of Fermented Foods , 2006 .

[7]  S. Ehrlich,et al.  A Phage Protein Confers Resistance to the Lactococcal Abortive Infection Mechanism AbiP , 2004, Journal of bacteriology.

[8]  T. Su,et al.  Interaction of the ocr gene 0.3 protein of bacteriophage T7 with EcoKI restriction/modification enzyme. , 2002, Nucleic acids research.

[9]  Boulnois Gj Genetics of capsular polysaccharide production in bacteria. , 1989 .

[10]  P. Su,et al.  Molecular Characterization of a New Abortive Infection System (AbiU) from Lactococcus lactisLL51-1 , 2001, Applied and Environmental Microbiology.

[11]  J. García-Martínez,et al.  Intervening Sequences of Regularly Spaced Prokaryotic Repeats Derive from Foreign Genetic Elements , 2005, Journal of Molecular Evolution.

[12]  Anders F. Andersson,et al.  Virus Population Dynamics and Acquired Virus Resistance in Natural Microbial Communities , 2008, Science.

[13]  S. Stirm Escherichia coli K Bacteriophages I. Isolation and Introductory Characterization of Five Escherichia coli K Bacteriophages , 1968, Journal of virology.

[14]  D. Dryden,et al.  The biology of restriction and anti-restriction. , 2005, Current opinion in microbiology.

[15]  I. Molineux,et al.  Role of the Gp16 lytic transglycosylase motif in bacteriophage T7 virions at the initiation of infection , 2000, Molecular microbiology.

[16]  E. Raleigh,et al.  Escherichia coli K-12 restricts DNA containing 5-methylcytosine. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Fedor V. Karginov,et al.  The CRISPR system: small RNA-guided defense in bacteria and archaea. , 2010, Molecular cell.

[18]  I. Molineux Host-parasite interactions: recent developments in the genetics of abortive phage infections. , 1991, The New biologist.

[19]  Nduka Okafor,et al.  Modern Industrial Microbiology and Biotechnology , 2007 .

[20]  C. Hill,et al.  Nucleotide sequence and distribution of the pTR2030 resistance determinant (hsp) which aborts bacteriophage infection in lactococci , 1990, Applied and environmental microbiology.

[21]  D. van Sinderen,et al.  Molecular Characterization of a Phage-Encoded Resistance System in Lactococcus lactis , 1999, Applied and Environmental Microbiology.

[22]  Madhavi Vuthoori,et al.  Transcriptional takeover by sigma appropriation: remodelling of the sigma70 subunit of Escherichia coli RNA polymerase by the bacteriophage T4 activator MotA and co-activator AsiA. , 2005, Microbiology.

[23]  J. Ferretti,et al.  Analysis of a second bacteriophage hyaluronidase gene from Streptococcus pyogenes: evidence for a third hyaluronidase involved in extracellular enzymatic activity , 1995, Infection and immunity.

[24]  R. Barrangou,et al.  CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes , 2007, Science.

[25]  B. Dreiseikelmann,et al.  The superimmunity gene sim of bacteriophage P1 causes superinfection exclusion. , 1989, Virology.

[26]  H. Engelberg-Kulka,et al.  Escherichia coli mazEF-mediated cell death as a defense mechanism that inhibits the spread of phage P1 , 2004, Molecular Genetics and Genomics.

[27]  R. Simons,et al.  Tropism switching in Bordetella bacteriophage defines a family of diversity-generating retroelements , 2004, Nature.

[28]  S. Ehrlich,et al.  Lactococcus lactis phage operon coding for an endonuclease homologous to RuvC , 1998, Molecular microbiology.

[29]  F. Studier,et al.  Analysis of bacteriophage T7 early RNAs and proteins on slab gels. , 1973, Journal of molecular biology.

[30]  M. Montagu,et al.  The ral gene of phage λ , 2004, Molecular and General Genetics MGG.

[31]  T. Wood,et al.  Exclusion of T4 phage by the hok/sok killer locus from plasmid R1 , 1996, Journal of bacteriology.

[32]  L. Schouls,et al.  Identification of genes that are associated with DNA repeats in prokaryotes , 2002, Molecular microbiology.

[33]  A. Campbell The future of bacteriophage biology , 2003, Nature Reviews Genetics.

[34]  B. Dreiseikelmann,et al.  The superinfection exclusion gene (sieA) of bacteriophage P22: identification and overexpression of the gene and localization of the gene product , 1995, Journal of bacteriology.

[35]  S. Steinbacher,et al.  Interaction of Salmonella Phage P22 with Its O-Antigen Receptor Studied by X-Ray Crystallography , 1997, Biological chemistry.

[36]  S. Moineau,et al.  Phenotypic and genetic characterization of the bacteriophage abortive infection mechanism AbiK from Lactococcus lactis , 1997, Applied and environmental microbiology.

[37]  L. Gold,et al.  The Rex system of bacteriophage lambda: tolerance and altruistic cell death. , 1992, Genes & development.

[38]  P. Taylor,et al.  Structure of Ocr from bacteriophage T7, a protein that mimics B-form DNA. , 2002, Molecular cell.

[39]  S. Iida,et al.  Two DNA antirestriction systems of bacteriophage P1, darA, and darB: characterization of darA- phages. , 1987, Virology.

[40]  L. Fortier,et al.  Expression and Site-Directed Mutagenesis of the Lactococcal Abortive Phage Infection Protein AbiK , 2005, Journal of bacteriology.

[41]  R. Utsumi Bacterial signal transduction : networks and drug targets , 2008 .

[42]  G. Salmond,et al.  Mutagenesis and Functional Characterization of the RNA and Protein Components of the toxIN Abortive Infection and Toxin-Antitoxin Locus of Erwinia , 2009, Journal of bacteriology.

[43]  J. García-Martínez,et al.  Short motif sequences determine the targets of the prokaryotic CRISPR defence system. , 2009, Microbiology.

[44]  F. Castillo,et al.  Localization and functional role of the pseudomonas bacteriophage 2 depolymerase , 1976, Journal of virology.

[45]  A. Pingoud,et al.  Type II restriction endonucleases: structure and mechanism , 2005, Cellular and Molecular Life Sciences.

[46]  Y. Stierhof,et al.  Location and unusual membrane topology of the immunity protein of the Escherichia coli phage T4 , 1993, Journal of virology.

[47]  E. Kjems Studies on streptococcal bacteriophages. I. Technique of isolating phage-producing strains. , 2009 .

[48]  I. Molineux,et al.  Incomplete entry of bacteriophage T7 DNA into F plasmid-containing Escherichia coli , 1995, Journal of bacteriology.

[49]  Stan J. J. Brouns,et al.  Small CRISPR RNAs Guide Antiviral Defense in Prokaryotes , 2008, Science.

[50]  D. Sinderen,et al.  Identification and characterization of phage‐resistance genes in temperate lactococcal bacteriophages , 2002, Molecular microbiology.

[51]  R. Gross,et al.  The BvgS/BvgA phosphorelay system of pathogenic Bordetellae: structure, function and evolution. , 2008, Advances in experimental medicine and biology.

[52]  U. Henning,et al.  Superinfection exclusion by T-even-type coliphages. , 1994, Trends in microbiology.

[53]  R. Barrangou,et al.  CRISPR/Cas, the Immune System of Bacteria and Archaea , 2010, Science.

[54]  C. Kleanthous,et al.  The Major Head Protein of Bacteriophage T4 Binds Specifically to Elongation Factor Tu* , 2000, The Journal of Biological Chemistry.

[55]  Phillip SanMiguel,et al.  Sequence analysis of Escherichia coli O157:H7 bacteriophage PhiV10 and identification of a phage-encoded immunity protein that modifies the O157 antigen. , 2009, FEMS microbiology letters.

[56]  F. Castillo,et al.  Studies on the Bacteriophage 2 Receptors of Pseudomonas aeruginosa , 1974, Journal of virology.

[57]  L. Black,et al.  A type IV modification dependent restriction nuclease that targets glucosylated hydroxymethyl cytosine modified DNAs. , 2007, Journal of molecular biology.

[58]  Shiraz A. Shah,et al.  Stygiolobus Rod-Shaped Virus and the Interplay of Crenarchaeal Rudiviruses with the CRISPR Antiviral System , 2008, Journal of bacteriology.

[59]  David J Weber,et al.  Restriction endonuclease inhibitor IPI* of bacteriophage T4: a novel structure for a dedicated target. , 2008, Journal of molecular biology.

[60]  Ian W. Sutherland,et al.  Polysaccharases for microbial exopolysaccharides , 1999 .

[61]  S. Ehrlich,et al.  Phage abortive infection mechanism from Lactococcus lactis subsp. lactis, expression of which is mediated by an Iso-ISS1 element , 1991, Applied and environmental microbiology.

[62]  Jeff F. Miller,et al.  Integration of multiple domains in a two‐component sensor protein: the Bordetella pertussis BvgAS phosphorelay. , 1996, The EMBO journal.

[63]  K. Makino,et al.  Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product , 1987, Journal of bacteriology.

[64]  E. Bidnenko,et al.  Phage abortive infection in lactococci: variations on a theme. , 2005, Current opinion in microbiology.

[65]  S. Ehrlich,et al.  The lactococcal abortive infection protein AbiP is membrane-anchored and binds nucleic acids. , 2008, Virology.

[66]  T. Bickle,et al.  Biology of DNA restriction. , 1993, Microbiological reviews.

[67]  G. Hanlon,et al.  Bacteriophages: an appraisal of their role in the treatment of bacterial infections. , 2007, International journal of antimicrobial agents.

[68]  T. Klaenhammer,et al.  Abortive Phage Resistance Mechanism AbiZ Speeds the Lysis Clock To Cause Premature Lysis of Phage-Infected Lactococcus lactis , 2006, Journal of bacteriology.

[69]  M. Eschbach,et al.  Evidence that TraT interacts with OmpA of Escherichia coli , 1986, FEBS letters.

[70]  L. Marraffini,et al.  CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea , 2010, Nature Reviews Genetics.

[71]  Jeff F. Miller,et al.  Diversity-generating retroelements. , 2007, Current opinion in microbiology.

[72]  Wenfang Wang,et al.  F exclusion of bacteriophage T7 occurs at the cell membrane. , 2004, Virology.

[73]  S. Moineau,et al.  Characterization of the Two-Component Abortive Phage Infection Mechanism AbiT from Lactococcus lactis , 2002, Journal of bacteriology.

[74]  N. Grishin,et al.  A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action , 2006, Biology Direct.

[75]  J. S. Godde,et al.  The Repetitive DNA Elements Called CRISPRs and Their Associated Genes: Evidence of Horizontal Transfer Among Prokaryotes , 2006, Journal of Molecular Evolution.

[76]  F. Studier,et al.  Inhibition of the type I restriction-modification enzymes EcoB and EcoK by the gene 0.3 protein of bacteriophage T7. , 1985, Journal of molecular biology.

[77]  T. Klaenhammer,et al.  Molecular characterization of a second abortive phage resistance gene present in Lactococcus lactis subsp. lactis ME2 , 1992, Journal of bacteriology.

[78]  L. Marraffini,et al.  CRISPR Interference Limits Horizontal Gene Transfer in Staphylococci by Targeting DNA , 2008, Science.

[79]  R. Gerardy-Schahn,et al.  Evolution of bacteriophages infecting encapsulated bacteria: lessons from Escherichia coli K1‐specific phages , 2006, Molecular microbiology.

[80]  S. Moineau,et al.  AbiQ, an Abortive Infection Mechanism fromLactococcus lactis , 1998, Applied and Environmental Microbiology.

[81]  R J Roberts,et al.  Restriction endonucleases. , 1976, CRC critical reviews in biochemistry.

[82]  Philippe Horvath,et al.  Phage Response to CRISPR-Encoded Resistance in Streptococcus thermophilus , 2007, Journal of bacteriology.

[83]  L. Snyder,et al.  The rex genes of bacteriophage lambda can inhibit cell function without phage superinfection. , 1989, Gene.

[84]  N. Murray,et al.  Restriction and modification systems. , 1991, Annual review of genetics.

[85]  G. Fitzgerald,et al.  Expression, Regulation, and Mode of Action of the AbiG Abortive Infection System of Lactococcus lactis subsp. cremoris UC653 , 1999, Applied and Environmental Microbiology.

[86]  I. Molineux,et al.  Genes 1.2 and 10 of bacteriophages T3 and T7 determine the permeability lesions observed in infected cells of Escherichia coli expressing the F plasmid gene pifA , 1991, Journal of bacteriology.

[87]  V. Georgiev Virology , 1955, Nature.

[88]  M. Mattey,et al.  Bacteriophage therapy--cooked goose or phoenix rising? , 2008, Current opinion in biotechnology.

[89]  T. Klaenhammer,et al.  Engineered bacteriophage-defence systems in bioprocessing , 2006, Nature Reviews Microbiology.

[90]  A. Hammad Evaluation of alginate‐encapsulated Azotobacter chroococcum as a phage‐resistant and an effective inoculum , 1998 .

[91]  Daniel H. Haft,et al.  A Guild of 45 CRISPR-Associated (Cas) Protein Families and Multiple CRISPR/Cas Subtypes Exist in Prokaryotic Genomes , 2005, PLoS Comput. Biol..

[92]  R. P. Ross,et al.  Bacteriophage and their lysins for elimination of infectious bacteria. , 2009, FEMS microbiology reviews.

[93]  S. Denyer,et al.  Reduction in Exopolysaccharide Viscosity as an Aid to Bacteriophage Penetration through Pseudomonas aeruginosa Biofilms , 2001, Applied and Environmental Microbiology.

[94]  D. van Sinderen,et al.  Identification and Characterization of Lactococcal-Prophage-Carried Superinfection Exclusion Genes , 2008, Applied and Environmental Microbiology.

[95]  S. Moineau,et al.  Microbiological and molecular impacts of AbiK on the lytic cycle of Lactococcus lactis phages of the 936 and P335 species. , 2000, Microbiology.

[96]  A. Hüttenhofer,et al.  Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[97]  R. Simons,et al.  Reverse Transcriptase-Mediated Tropism Switching in Bordetella Bacteriophage , 2002, Science.

[98]  G. O’Toole,et al.  Interaction between Bacteriophage DMS3 and Host CRISPR Region Inhibits Group Behaviors of Pseudomonas aeruginosa , 2008, Journal of bacteriology.

[99]  A. Forsgren,et al.  Effect of Protein A on Adsorption of Bacteriophages to Staphylococcus aureus , 1974, Journal of virology.

[100]  G. Fitzgerald,et al.  Cloning and DNA sequence analysis of two abortive infection phage resistance determinants from the lactococcal plasmid pNP40 , 1995, Applied and environmental microbiology.

[101]  D. Sinderen,et al.  Prophage-Like Elements in Bifidobacteria: Insights from Genomics, Transcription, Integration, Distribution, and Phylogenetic Analysis , 2005, Applied and Environmental Microbiology.

[102]  M. Fenner,et al.  CRISPR--a widespread system that provides acquired resistance against phages in bacteria and archaea. , 2007 .

[103]  E. Kjems Studies on streptococcal bacteriophages. 5. Serological investigation of phages isolated from 91 strains of group A haemolytic streptococci. , 2009, Acta pathologica et microbiologica Scandinavica.

[104]  D. Rao,et al.  S-Adenosyl-L-methionine–Dependent Restriction Enzymes , 2004, Critical reviews in biochemistry and molecular biology.

[105]  B. Dreiseikelmann,et al.  The sim gene of Escherichia coli phage P1: nucleotide sequence and purification of the processed protein. , 1990, Virology.

[106]  S. Moineau,et al.  Lactococcal Phage Genes Involved in Sensitivity to AbiK and Their Relation to Single-Strand Annealing Proteins , 2004, Journal of bacteriology.

[107]  G. Kaufmann Anticodon nucleases. , 2000, Trends in biochemical sciences.

[108]  P. Toothman Restriction alleviation by bacteriophages lambda and lambda reverse , 1981, Journal of virology.

[109]  J. Morris,et al.  Bacteriophage Therapy , 2001, Antimicrobial Agents and Chemotherapy.

[110]  R. Morgan Genetics and molecular biology. , 1995, Current opinion in lipidology.

[111]  G Vergnaud,et al.  CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. , 2005, Microbiology.

[112]  Philippe Horvath,et al.  Diversity, Activity, and Evolution of CRISPR Loci in Streptococcus thermophilus , 2007, Journal of bacteriology.

[113]  L. Snyder Phage‐exclusion enzymes: a bonanza of biochemical and cell biology reagents? , 1995, Molecular microbiology.

[114]  S. Ehrlich,et al.  Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. , 2005, Microbiology.

[115]  C. Cooney,et al.  Polysaccharide lyases , 1986, Applied biochemistry and biotechnology.

[116]  Roger W. Hendrix,et al.  Phage Genomics Small Is Beautiful , 2002, Cell.

[117]  S. Ehrlich,et al.  The Lactococcal Abortive Phage Infection System AbiP Prevents both Phage DNA Replication and Temporal Transcription Switch , 2004, Journal of bacteriology.

[118]  E. Norrby Nobel Prizes and the emerging virus concept , 2008, Archives of Virology.

[119]  Erik J. Sontheimer,et al.  Self vs. non-self discrimination during CRISPR RNA-directed immunity , 2009, Nature.

[120]  N. Murray,et al.  Restriction alleviation and modification enhancement by the Rac prophage of Escherichia coli K‐12 , 1995, Molecular microbiology.

[121]  M. Wessels,et al.  Relative contributions of hyaluronic acid capsule and M protein to virulence in a mucoid strain of the group A Streptococcus , 1997, Infection and immunity.

[122]  T. Foster Immune evasion by staphylococci , 2005, Nature Reviews Microbiology.

[123]  F. Studier,et al.  SAMase gene of bacteriophage T3 is responsible for overcoming host restriction , 1976, Journal of virology.

[124]  Kathryn S. Lilley,et al.  The phage abortive infection system, ToxIN, functions as a protein–RNA toxin–antitoxin pair , 2009, Proceedings of the National Academy of Sciences.

[125]  R. Garrett,et al.  Identification of novel non‐coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus , 2004, Molecular microbiology.

[126]  R. Magnuson Hypothetical Functions of Toxin-Antitoxin Systems , 2007, Journal of bacteriology.

[127]  H. Neve,et al.  The ltp gene of temperate Streptococcus thermophilus phage TP-J34 confers superinfection exclusion to Streptococcus thermophilus and Lactococcus lactis. , 2006, Virology.

[128]  H. Smith,et al.  Abolition of DNA recognition site resistance to the restriction endonuclease EcoRII. , 1988, Biomedica biochimica acta.

[129]  S. Duquesne,et al.  The iron-siderophore transporter FhuA is the receptor for the antimicrobial peptide microcin J25: role of the microcin Val11-Pro16 beta-hairpin region in the recognition mechanism. , 2005, The Biochemical journal.

[130]  C. Hill,et al.  The Lactococcal Plasmid pNP40 Encodes a Third Bacteriophage Resistance Mechanism, One Which Affects Phage DNA Penetration , 1996, Applied and environmental microbiology.

[131]  A. Piekarowicz,et al.  The role of Dam methylation in phase variation of Haemophilus influenzae genes involved in defence against phage infection. , 2005, Microbiology.

[132]  M. Montagu,et al.  The ral gene of phage λ , 2004, Molecular and General Genetics MGG.

[133]  Dalin Rifat,et al.  Exclusion of glucosyl-hydroxymethylcytosine DNA containing bacteriophages is overcome by the injected protein inhibitor IPI*. , 2007, Journal of molecular biology.