Abortive Infection: Bacterial Suicide as an Antiviral Immune Strategy.

Facing frequent phage challenges, bacteria have evolved numerous mechanisms to resist phage infection. A commonly used phage resistance strategy is abortive infection (Abi), in which the infected cell commits suicide before the phage can complete its replication cycle. Abi prevents the phage epidemic from spreading to nearby cells, thus protecting the bacterial colony. The Abi strategy is manifested by a plethora of mechanistically diverse defense systems that are abundant in bacterial genomes. In turn, phages have developed equally diverse mechanisms to overcome bacterial Abi. This review summarizes the current knowledge on bacterial defense via cell suicide. It describes the principles of Abi, details how these principles are implemented in a variety of natural defense systems, and discusses phage counter-defense mechanisms. Expected final online publication date for the Annual Review of Virology, Volume 7 is September 29, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

[1]  M. F. White,et al.  An anti-CRISPR viral ring nuclease subverts type III CRISPR immunity , 2020, Nature.

[2]  R. Sorek,et al.  The pan-immune system of bacteria: antiviral defence as a community resource , 2019, Nature Reviews Microbiology.

[3]  Gil Amitai,et al.  Cyclic GMP–AMP signalling protects bacteria against viral infection , 2019, Nature.

[4]  P. J. Kranzusch,et al.  Structure and mechanism of a cyclic trinucleotide-activated bacterial endonuclease mediating bacteriophage immunity , 2019, bioRxiv.

[5]  Mohit M. Jain,et al.  HORMA domain proteins and a Pch2-like ATPase regulate bacterial cGAS-like enzymes to mediate bacteriophage immunity , 2019, bioRxiv.

[6]  J. Bondy-Denomy,et al.  Cas13 Helps Bacteria Play Dead when the Enemy Strikes. , 2019, Cell Host and Microbe.

[7]  L. Marraffini,et al.  Cas13-induced cellular dormancy prevents the rise of CRISPR-resistant bacteriophage , 2019, Nature.

[8]  M. F. White,et al.  A Type III CRISPR Ancillary Ribonuclease Degrades Its Cyclic Oligoadenylate Activator , 2019, bioRxiv.

[9]  G. Hatfull,et al.  More Evidence of Collusion: a New Prophage-Mediated Viral Defense System Encoded by Mycobacteriophage Sbash , 2019, mBio.

[10]  G. Hatfull,et al.  Yet More Evidence of Collusion: a New Viral Defense System Encoded by Gordonia Phage CarolAnn , 2019, mBio.

[11]  L. Marraffini,et al.  (Ph)ighting Phages: How Bacteria Resist Their Parasites. , 2019, Cell host & microbe.

[12]  P. J. Kranzusch,et al.  Bacterial cGAS-like enzymes synthesize diverse nucleotide signals , 2019, Nature.

[13]  K. Maxwell,et al.  A chemical defence against phage infection , 2018, Nature.

[14]  C. Waters,et al.  Direct activation of a phospholipase by cyclic GMP-AMP in El Tor Vibrio cholerae , 2018, Proceedings of the National Academy of Sciences.

[15]  T. Wood,et al.  Post-segregational Killing and Phage Inhibition Are Not Mediated by Cell Death Through Toxin/Antitoxin Systems , 2018, Front. Microbiol..

[16]  M. D. de Jonge,et al.  For the greater good: Programmed cell death in bacterial communities. , 2018, Microbiological research.

[17]  Česlovas Venclovas,et al.  A cyclic oligonucleotide signaling pathway in type III CRISPR-Cas systems , 2017, Science.

[18]  Rotem Sorek,et al.  Intracellular signaling in CRISPR-Cas defense , 2017, Science.

[19]  Frank Schwede,et al.  Type III CRISPR–Cas systems produce cyclic oligoadenylate second messengers , 2017, Nature.

[20]  H. Molina,et al.  A Eukaryotic-like Serine/Threonine Kinase Protects Staphylococci against Phages. , 2016, Cell host & microbe.

[21]  A. Buckling,et al.  Evolutionary Ecology of Prokaryotic Immune Mechanisms , 2016, Microbiology and Molecular Reviews.

[22]  Česlovas Venclovas,et al.  Spatiotemporal Control of Type III-A CRISPR-Cas Immunity: Coupling DNA Degradation with the Target RNA Recognition. , 2016, Molecular cell.

[23]  L. Aravind,et al.  Comparative genomic analyses reveal a vast, novel network of nucleotide-centric systems in biological conflicts, immunity and signaling , 2015, Nucleic acids research.

[24]  Luciano A. Marraffini,et al.  CRISPR-Cas immunity in prokaryotes , 2015, Nature.

[25]  Sita J. Saunders,et al.  An updated evolutionary classification of CRISPR–Cas systems , 2015, Nature Reviews Microbiology.

[26]  Eric C Keen,et al.  A century of phage research: Bacteriophages and the shaping of modern biology , 2015, BioEssays : news and reviews in molecular, cellular and developmental biology.

[27]  Peter C. Fineran,et al.  Remarkable Mechanisms in Microbes to Resist Phage Infections. , 2014, Annual review of virology.

[28]  Peter C. Fineran,et al.  A widespread bacteriophage abortive infection system functions through a Type IV toxin–antitoxin mechanism , 2014, Nucleic acids research.

[29]  Rotem Sorek,et al.  CRISPR-mediated adaptive immune systems in bacteria and archaea. , 2013, Annual review of biochemistry.

[30]  R. Bertram,et al.  Toxin-antitoxin systems are ubiquitous and versatile modulators of prokaryotic cell fate. , 2013, FEMS microbiology letters.

[31]  E. Koonin,et al.  Live virus-free or die: coupling of antivirus immunity and programmed suicide or dormancy in prokaryotes , 2012, Biology Direct.

[32]  G. Salmond,et al.  Viral Evasion of a Bacterial Suicide System by RNA–Based Molecular Mimicry Enables Infectious Altruism , 2012, PLoS genetics.

[33]  J. Mekalanos,et al.  Coordinated Regulation of Accessory Genetic Elements Produces Cyclic Di-Nucleotides for V. cholerae Virulence , 2012, Cell.

[34]  T. Yonesaki,et al.  Dmd of bacteriophage T4 functions as an antitoxin against Escherichia coli LsoA and RnlA toxins , 2012, Molecular microbiology.

[35]  A. Sasaki,et al.  Success of a suicidal defense strategy against infection in a structured habitat , 2012, Scientific Reports.

[36]  T. Wood,et al.  Toxin-Antitoxin Systems Influence Biofilm and Persister Cell Formation and the General Stress Response , 2011, Applied and Environmental Microbiology.

[37]  R. Terns,et al.  CRISPR-based adaptive immune systems. , 2011, Current opinion in microbiology.

[38]  Raphaël Leplae,et al.  Diversity of bacterial type II toxin–antitoxin systems: a comprehensive search and functional analysis of novel families , 2011, Nucleic acids research.

[39]  Peter C. Fineran,et al.  A processed noncoding RNA regulates an altruistic bacterial antiviral system , 2011, Nature Structural &Molecular Biology.

[40]  S. Lemire,et al.  Escherichia coli rnlA and rnlB Compose a Novel Toxin–Antitoxin System , 2011, Genetics.

[41]  Sylvain Moineau,et al.  Bacteriophage resistance mechanisms , 2010, Nature Reviews Microbiology.

[42]  J. Cox,et al.  Comprehensive Functional Analysis of Mycobacterium tuberculosis Toxin-Antitoxin Systems: Implications for Pathogenesis, Stress Responses, and Evolution , 2009, PLoS genetics.

[43]  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.

[44]  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.

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

[46]  K. Lewis,et al.  Specialized Persister Cells and the Mechanism of Multidrug Tolerance in Escherichia coli , 2004, Journal of bacteriology.

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

[48]  R. Slavcev,et al.  Stationary phase-like properties of the bacteriophage λ Rex exclusion phenotype , 2003, Molecular Genetics and Genomics.

[49]  K. Gerdes,et al.  RelE, a global inhibitor of translation, is activated during nutritional stress , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[52]  F. Repoila,et al.  The genome of the pseudo T-even bacteriophages, a diverse group that resembles T4. , 1997, Journal of molecular biology.

[53]  T. Kai,et al.  Destabilization of bacteriophage T4 mRNAs by a mutation of gene 61.5. , 1996, Genetics.

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

[55]  M. Sprinzl,et al.  Elongation factor Tu: a regulatory GTPase with an integrated effector. , 1994, Trends in biochemical sciences.

[56]  T. Bickle,et al.  The Escherichia coli prr region encodes a functional type IC DNA restriction system closely integrated with an anticodon nuclease gene. , 1994, Journal of molecular biology.

[57]  L. Snyder,et al.  Translation elongation factor Tu cleaved by a phage-exclusion system. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[58]  G. Kaufmann,et al.  HSD restriction‐modification proteins partake in latent anticodon nuclease. , 1992, EMBO Journal.

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

[60]  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.

[61]  I. Molineux,et al.  Expression of gene 1.2 and gene 10 of bacteriophage T7 is lethal to F plasmid-containing Escherichia coli , 1991, Journal of bacteriology.

[62]  T. Klaenhammer,et al.  Plasmid-induced abortive infection in lactococci: a review. , 1990 .

[63]  R. Levitz,et al.  The optional E. coli prr locus encodes a latent form of phage T4‐induced anticodon nuclease. , 1990, The EMBO journal.

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

[65]  G. Kaufmann,et al.  In vitro reconstitution of anticodon nuclease from components encoded by phage T4 and Escherichia coli CTr5X. , 1989, EMBO Journal.

[66]  J. P. Condreay,et al.  Mutants of bacteriophage T7 that escape F restriction. , 1989, Journal of molecular biology.

[67]  L. Snyder,et al.  The lit gene product which blocks bacteriophage T4 late gene expression is a membrane protein encoded by a cryptic DNA element, e14 , 1988, Journal of bacteriology.

[68]  L. Gold,et al.  Wild-type bacteriophage T4 is restricted by the lambda rex genes , 1987, Journal of virology.

[69]  R. Levitz,et al.  Bacteriophage T4 anticodon nuclease, polynucleotide kinase and RNA ligase reprocess the host lysine tRNA. , 1987, The EMBO journal.

[70]  S. Molin,et al.  Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[71]  M. David,et al.  Phage and host genetic determinants of the specific anticodon loop cleavages in bacteriophage T4-infected Escherichia coli CTr5X. , 1986, Journal of molecular biology.

[72]  M. Malamy,et al.  Identification of the pifC gene and its role in negative control of F factor pif gene expression , 1983, Journal of bacteriology.

[73]  J. Clément,et al.  Genetic study of a membrane protein: DNA sequence alterations due to 17 lamB point mutations affecting adsorption of phage lambda. , 1983, The EMBO journal.

[74]  M. David,et al.  T4 bacteriophage-coded polynucleotide kinase and RNA ligase are involved in host tRNA alteration or repair. , 1982, Virology.

[75]  M. Kröger,et al.  The rex region of bacteriophage lambda: two genes under three-way control. , 1982, Gene.

[76]  L. Snyder,et al.  The gol site: a cis-acting bacteriophage T4 regulatory region that can affect expression of all the T4 late genes. , 1982, Journal of molecular biology.

[77]  D. Duckworth,et al.  Inhibition of bacteriophage replication by extrachromosomal genetic elements. , 1981, Microbiological reviews.

[78]  I. Herskowitz,et al.  Rex-dependent exclusion of lambdoid phages. II. Determinants of sensitivity to exclusion. , 1980, Virology.

[79]  K. Sirotkin,et al.  A new gene of Escherichia coli K-12 whose product participates in T4 bacteriophage late gene expression: interaction of lit with the T4-induced polynucleotide 5'-kinase 3'-phosphatase , 1979, Journal of bacteriology.

[80]  S. Svenson,et al.  Bacteriophage T4-induced shut-off of host-specific translation , 1976, Journal of virology.

[81]  N. Cozzarelli,et al.  Genetics and Physiology of Bacteriophage T4 3′-Phosphatase: Evidence for Involvement of the Enzyme in T4 DNA Metabolism , 1974, Journal of virology.

[82]  W. Hamilton The genetical evolution of social behaviour. I. , 1964, Journal of theoretical biology.

[83]  S. Benzer,et al.  FINE STRUCTURE OF A GENETIC REGION IN BACTERIOPHAGE. , 1955, Proceedings of the National Academy of Sciences of the United States of America.

[84]  Jacqueline,et al.  Prophage-mediated defense against viral attack and viral counter-defense , 2017 .

[85]  Česlovas Venclovas,et al.  Type III CRISPR-Cas Immunity: Major Differences Brushed Aside. , 2017, Trends in microbiology.

[86]  R. Barrangou,et al.  Lactic Acid Bacteria Defenses Against Phages , 2011 .

[87]  G. Fitzgerald,et al.  Bacteriophage defence systems in lactic acid bacteria , 2004, Antonie van Leeuwenhoek.

[88]  T. Yonesaki,et al.  Destabilization of Bacteriophage T 4 mRNAs by a Mutation of Gene 61 , 2002 .