1932

Abstract

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.

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2020-09-29
2024-04-23
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Literature Cited

  1. 1. 
    Rostøl JT, Marraffini L. 2019. (Ph)ighting phages: how bacteria resist their parasites. Cell Host Microbe 25:184–94
    [Google Scholar]
  2. 2. 
    Bernheim A, Sorek R. 2020. The pan-immune system of bacteria: antiviral defence as a community resource. Nat. Rev. Microbiol. 18:113–19
    [Google Scholar]
  3. 3. 
    Dy RL, Richter C, Salmond GPC, Fineran PC 2014. Remarkable mechanisms in microbes to resist phage infections. Annu. Rev. Virol. 1:307–31
    [Google Scholar]
  4. 4. 
    Clément JM, Lepouce E, Marchal C, Hofnung M 1983. Genetic study of a membrane protein: DNA sequence alterations due to 17 lamB point mutations affecting adsorption of phage lambda. EMBO J 2:177–80
    [Google Scholar]
  5. 5. 
    Kronheim S, Daniel-Ivad M, Duan Z, Hwang S, Wong AI et al. 2018. A chemical defence against phage infection. Nature 564:7735283–86
    [Google Scholar]
  6. 6. 
    Duckworth DH, Glenn J, McCorquodale DJ 1981. Inhibition of bacteriophage replication by extrachromosomal genetic elements. Microbiol. Rev. 45:152–71
    [Google Scholar]
  7. 7. 
    Peeters SH, de Jonge MI 2018. For the greater good: programmed cell death in bacterial communities. Microbiol. Res. 207:161–69
    [Google Scholar]
  8. 8. 
    Hamilton WD. 1964. The genetical evolution of social behaviour. I. J. Theor. Biol. 7:11–16
    [Google Scholar]
  9. 9. 
    Van Houte S, Buckling A, Westra ER 2016. Evolutionary ecology of prokaryotic immune mechanisms. Microbiol. Mol. Biol. Rev. 80:3745–63
    [Google Scholar]
  10. 10. 
    Fukuyo M, Sasaki A, Kobayashi I 2012. Success of a suicidal defense strategy against infection in a structured habitat. Sci. Rep. 2:238
    [Google Scholar]
  11. 11. 
    Forde A, Fitzgerald GF. 1999. Bacteriophage defence systems in lactic acid bacteria. Antonie Van Leeuwenhoek 76:1–489–113
    [Google Scholar]
  12. 12. 
    Snyder L. 1995. Phage-exclusion enzymes: a bonanza of biochemical and cell biology reagents. ? Mol. Microbiol. 15:3415–20
    [Google Scholar]
  13. 13. 
    Schmitt CK, Molineux IJ. 1991. Expression of gene 1.2 and gene 10 of bacteriophage T7 is lethal to F plasmid-containing Escherichia coli. . J. Bacteriol 173:41536–43
    [Google Scholar]
  14. 14. 
    Bingham R, Ekunwe SI, Falk S, Snyder L, Kleanthous C 2000. The major head protein of bacteriophage T4 binds specifically to elongation factor Tu. J. Biol. Chem. 275:3023219–26
    [Google Scholar]
  15. 15. 
    Depardieu F, Didier J-P, Bernheim A, Sherlock A, Molina H et al. 2016. A eukaryotic-like serine/threonine kinase protects Staphylococci against phages. Cell Host Microbe 20:4471–81
    [Google Scholar]
  16. 16. 
    Durmaz E, Klaenhammer TR. 2007. Abortive phage resistance mechanism AbiZ speeds the lysis clock to cause premature lysis of phage-infected Lactococcus lactis. J. . Bacteriol 189:41417–25
    [Google Scholar]
  17. 17. 
    Kazlauskiene M, Kostiuk G, Venclovas Č, Tamulaitis G, Siksnys V 2017. A cyclic oligonucleotide signaling pathway in type III CRISPR-Cas systems. Science 357:6351605–9
    [Google Scholar]
  18. 18. 
    Niewoehner O, Garcia-Doval C, Rostøl JT, Berk C, Schwede F et al. 2017. Type III CRISPR-Cas systems produce cyclic oligoadenylate second messengers. Nature 548:7669543–48
    [Google Scholar]
  19. 19. 
    Koga M, Otsuka Y, Lemire S, Yonesaki T 2011. Escherichia coli rnlA and rnlB compose a novel toxin–antitoxin system. Genetics 187:1123–30
    [Google Scholar]
  20. 20. 
    Cohen D, Melamed S, Millman A, Shulman G, Oppenheimer-Shaanan Y et al. 2019. Cyclic GMP-AMP signalling protects bacteria against viral infection. Nature 574:7780691–95
    [Google Scholar]
  21. 21. 
    Parma DH, Snyder M, Sobolevski S, Nawroz M, Brody E, Gold L 1992. The Rex system of bacteriophage lambda: tolerance and altruistic cell death. Genes Dev 6:3497–510
    [Google Scholar]
  22. 22. 
    Schmitt CK, Kemp P, Molineux IJ 1991. 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. . J. Bacteriol 173:206507–14
    [Google Scholar]
  23. 23. 
    Lau RK, Ye Q, Birkholz EA, Berg KR, Patel L et al. 2020. Structure and mechanism of a cyclic trinucleotide-activated bacterial endonuclease mediating bacteriophage immunity. Mol. Cell 77:4723–33
    [Google Scholar]
  24. 24. 
    Levitz R, Chapman D, Amitsur M, Green R, Snyder L, Kaufmann G 1990. The optional E. coli prr locus encodes a latent form of phage T4-induced anticodon nuclease. EMBO J 9:51383–89
    [Google Scholar]
  25. 25. 
    Yu YT, Snyder L. 1994. Translation elongation factor Tu cleaved by a phage-exclusion system. PNAS 91:2802–6
    [Google Scholar]
  26. 26. 
    Otsuka Y, Yonesaki T. 2012. Dmd of bacteriophage T4 functions as an antitoxin against Escherichia coli LsoA and RnlA toxins. Mol. Microbiol. 83:4669–81
    [Google Scholar]
  27. 27. 
    Fineran PC, Blower TR, Foulds IJ, Humphreys DP, Lilley KS, Salmond GPC 2009. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. PNAS 106:3894–99
    [Google Scholar]
  28. 28. 
    Slavcev RA, Hayes S. 2003. Stationary phase-like properties of the bacteriophage λ Rex exclusion phenotype. Mol. Genet. Genom. 269:140–48
    [Google Scholar]
  29. 29. 
    Makarova KS, Anantharaman V, Aravind L, Koonin EV 2012. Live virus-free or die: coupling of antivirus immunity and programmed suicide or dormancy in prokaryotes. Biol. Direct 7:40
    [Google Scholar]
  30. 30. 
    Keen EC. 2015. A century of phage research: bacteriophages and the shaping of modern biology. Bioessays 37:16–9
    [Google Scholar]
  31. 31. 
    Sing WD, Klaenhammer TR. 1990. Plasmid-induced abortive infection in lactococci: a review. J. Dairy Sci. 73:92239–51
    [Google Scholar]
  32. 32. 
    Chopin M-C, Chopin A, Bidnenko E 2005. Phage abortive infection in lactococci: variations on a theme. Curr. Opin. Microbiol. 8:4473–79
    [Google Scholar]
  33. 33. 
    Barrangou R, Horvath P. 2011. Lactic acid bacteria defenses against phages. Stress Responses of Lactic Acid Bacteria E Tsakalidou, K Papadimitriou 459–78 Boston, MA: Springer US
    [Google Scholar]
  34. 34. 
    Benzer S. 1955. Fine structure of a genetic region in bacteriophage. PNAS 41:6344–54
    [Google Scholar]
  35. 35. 
    Landsmann J, Kroger M, Hobom G 1982. The rex region of bacteriophage lambda: two genes under three-way control. Gene 20:111–24
    [Google Scholar]
  36. 36. 
    Snyder L, McWilliams K. 1989. The rex genes of bacteriophage lambda can inhibit cell function without phage superinfection. Gene 81:117–24
    [Google Scholar]
  37. 37. 
    Toothman P, Herskowitz I. 1980. Rex-dependent exclusion of lambdoid phages. II. Determinants of sensitivity to exclusion. Virology 102:1147–60
    [Google Scholar]
  38. 38. 
    Shinedling S, Parma D, Gold L 1987. Wild-type bacteriophage T4 is restricted by the lambda rex genes. J. Virol. 61:123790–94
    [Google Scholar]
  39. 39. 
    Cheng X, Wang W, Molineux IJ 2004. F exclusion of bacteriophage T7 occurs at the cell membrane. Virology 326:2340–52
    [Google Scholar]
  40. 40. 
    Miller JF, Malamy MH. 1983. Identification of the pifC gene and its role in negative control of F factor pif gene expression. J. Bacteriol. 156:1338–47
    [Google Scholar]
  41. 41. 
    Dy RL, Przybilski R, Semeijn K, Salmond GPC, Fineran PC 2014. A widespread bacteriophage abortive infection system functions through a Type IV toxin-antitoxin mechanism. Nucleic Acids Res 42:74590–605
    [Google Scholar]
  42. 42. 
    Molineux IJ, Schmitt CK, Condreay JP 1989. Mutants of bacteriophage T7 that escape F restriction. J. Mol. Biol. 207:3563–74
    [Google Scholar]
  43. 43. 
    Kao C, Snyder L. 1988. The lit gene product which blocks bacteriophage T4 late gene expression is a membrane protein encoded by a cryptic DNA element, e14. J. Bacteriol. 170:52056–62
    [Google Scholar]
  44. 44. 
    Cooley W, Sirotkin K, Green R, Synder L 1979. 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. J. Bacteriol. 140:183–91
    [Google Scholar]
  45. 45. 
    Sprinzl M. 1995. Elongation factor Tu: a regulatory GTPase with an integrated effector. Trends Biochem. Sci. 19:245–50
    [Google Scholar]
  46. 46. 
    Champness WC, Snyder L. 1982. The gol site: a Cis-acting bacteriophage T4 regulatory region that can affect expression of all the T4 late genes. J. Mol. Biol. 155:4395–407
    [Google Scholar]
  47. 47. 
    Monod C, Repoila F, Kutateladze M, Tétart F, Krisch H 1997. The genome of the pseudo T-even bacteriophages, a diverse group that resembles T4. J. Mol. Biol. 267:2237–49
    [Google Scholar]
  48. 48. 
    Depew RE, Cozzarelli NR. 1974. Genetics and physiology of bacteriophage T4 3′-phosphatase: evidence for involvement of the enzyme in T4 DNA metabolism. J. Virol. 13:4888–97
    [Google Scholar]
  49. 49. 
    Kaufmann G, David M, Borasio GD, Teichmann A, Paz A et al. 1986. Phage and host genetic determinants of the specific anticodon loop cleavages in bacteriophage T4-infected Escherichia coli CTr5X. J. Mol. Biol. 188:115–22
    [Google Scholar]
  50. 50. 
    Tyndall C, Meister J, Bickle TA 1994. The Escherichia coli prr region encodes a functional type IC DNA restriction system closely integrated with an anticodon nutlease gene. J. Mol. Biol. 237:3266–74
    [Google Scholar]
  51. 51. 
    Amitsur M, Morad I, Kaufmann G 1989. In vitro reconstitution of anticodon nuclease from components encoded by phage T4 and Escherichia coli CTr5X. EMBO J 8:82411–15
    [Google Scholar]
  52. 52. 
    Amitsur M, Morad I, Chapman-Shimshoni D, Kaufmann G 1992. HSD restriction-modification proteins partake in latent anticodon nuclease. EMBO J 11:83129–34
    [Google Scholar]
  53. 53. 
    Amitsur M, Levitz R, Kaufmann G 1987. Bacteriophage T4 anticodon nuclease, polynucleotide kinase and RNA ligase reprocess the host lysine tRNA. EMBO J 6:82499–503
    [Google Scholar]
  54. 54. 
    David M, Borasio GD, Kaufmann G 1982. T4 bacteriophage-coded polynucleotide kinase and RNA ligase are involved in host tRNA alteration and repair. Virology 123:2480–83
    [Google Scholar]
  55. 55. 
    Unterholzner SJ, Poppenberger B, Rozhon W 2013. Toxin-antitoxin systems: biology, identification, and application. Mob. Genet. Elements 3:5e26219
    [Google Scholar]
  56. 56. 
    Leplae R, Geeraerts D, Hallez R, Guglielmini J, Drèze P, Van Melderen L 2011. Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Res 39:135513–25
    [Google Scholar]
  57. 57. 
    Schuster CF, Bertram R. 2013. Toxin-antitoxin systems are ubiquitous and versatile modulators of prokaryotic cell fate. FEMS Microbiol. Lett. 340:273–85
    [Google Scholar]
  58. 58. 
    Ramage HR, Connolly LE, Cox JS 2009. Comprehensive functional analysis of Mycobacterium tuberculosis toxin-antitoxin systems: implications for pathogenesis, stress responses, and evolution. PLOS Genet 5:12e1000767
    [Google Scholar]
  59. 59. 
    Christensen SK, Mikkelsen M, Pedersen K, Gerdes K 2001. RelE, a global inhibitor of translation, is activated during nutritional stress. PNAS 98:2514328–33
    [Google Scholar]
  60. 60. 
    Keren I, Shah D, Spoering A, Kaldalu N, Lewis K 2004. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. . Bacteriol 186:248172–80
    [Google Scholar]
  61. 61. 
    Wang X, Wood TK. 2011. Toxin-antitoxin systems influence biofilm and persister cell formation and the general stress response. Appl. Environ. Microbiol. 77:165577–83
    [Google Scholar]
  62. 62. 
    Gerdes K, Rasmussen PB, Molin S 1986. Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. PNAS 83:103116–20
    [Google Scholar]
  63. 63. 
    Song S, Wood TK. 2018. Post-segregational killing and phage inhibition are not mediated by cell death through toxin/antitoxin systems. Front. Microbiol. 9:814
    [Google Scholar]
  64. 64. 
    Svenson SB, Karlström OH. 1976. Bacteriophage T4-induced shut-off of host-specific translation. J. Virol. 17:2326–34
    [Google Scholar]
  65. 65. 
    Kai T, Selick HE, Yonesaki T 1996. Destabilization of bacteriophage T4 mRNAs by a mutation of gene 61.5. . Genetics 144:17–14
    [Google Scholar]
  66. 66. 
    Emond E, Dion E, Walker SA, Vedamuthu ER, Kondo JK, Moineau S 1998. AbiQ, an abortive infection mechanism from Lactococcus lactis. Appl. Environ. . Microbiol 64:124748–56
    [Google Scholar]
  67. 67. 
    Blower TR, Pei XY, Short FL, Fineran PC, Humphreys DP et al. 2011. A processed noncoding RNA regulates an altruistic bacterial antiviral system. Nat. Struct. Mol. Biol. 18:2185–90
    [Google Scholar]
  68. 68. 
    Blower TR, Evans TJ, Przybilski R, Fineran PC, Salmond GPC 2012. Viral evasion of a bacterial suicide system by RNA-based molecular mimicry enables infectious altruism. PLOS Genet 8:10e1003023
    [Google Scholar]
  69. 69. 
    Davies BW, Bogard RW, Young TS, Mekalanos JJ 2012. Coordinated regulation of accessory genetic elements produces cyclic di-nucleotides for V. cholerae virulence. Cell 149:2358–70
    [Google Scholar]
  70. 70. 
    Severin GB, Ramliden MS, Hawver LA, Wang K, Pell ME et al. 2018. Direct activation of a phospholipase by cyclic GMP-AMP in El Tor Vibrio cholerae. . PNAS 115:26E6048–6048
    [Google Scholar]
  71. 71. 
    Whiteley AT, Eaglesham JB, de Oliveira Mann CC, Morehouse BR, Lowey B et al. 2019. Bacterial cGAS-like enzymes synthesize diverse nucleotide signals. Nature 567:7747194–99
    [Google Scholar]
  72. 72. 
    Ye Q, Lau RK, Mathews IT, Birkholz EA, Watrous JD et al. 2020. HORMA domain proteins and a Trip13-like ATPase regulate bacterial cGAS-like enzymes to mediate bacteriophage immunity. Mol. Cell 77:4709–22
    [Google Scholar]
  73. 73. 
    Burroughs AM, Zhang D, Schäffer DE, Iyer LM, Aravind L 2015. Comparative genomic analyses reveal a vast, novel network of nucleotide-centric systems in biological conflicts, immunity and signaling. Nucleic Acids Res 43:2210633–54
    [Google Scholar]
  74. 74. 
    Sorek R, Lawrence CM, Wiedenheft B 2013. CRISPR-mediated adaptive immune systems in bacteria and archaea. Annu. Rev. Biochem. 82:237–66
    [Google Scholar]
  75. 75. 
    Terns MP, Terns RM. 2011. CRISPR-based adaptive immune systems. Curr. Opin. Microbiol. 14:3321–27
    [Google Scholar]
  76. 76. 
    Marraffini LA. 2015. CRISPR-Cas immunity in prokaryotes. Nature 526:757155–61
    [Google Scholar]
  77. 77. 
    Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA et al. 2015. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13:11722–36
    [Google Scholar]
  78. 78. 
    Tamulaitis G, Venclovas Č, Siksnys V 2017. Type III CRISPR-Cas immunity: major differences brushed aside. Trends Microbiol 25:149–61
    [Google Scholar]
  79. 79. 
    Kazlauskiene M, Tamulaitis G, Kostiuk G, Venclovas Č, Siksnys V 2016. Spatiotemporal control of type III-A CRISPR-Cas immunity: coupling DNA degradation with the target RNA recognition. Mol. Cell 62:2295–306
    [Google Scholar]
  80. 80. 
    Liu TY, Iavarone AT, Doudna JA 2017. RNA and DNA targeting by a reconstituted Thermus thermophilus type III-A CRISPR-Cas system. PLOS ONE 12:1e0170552
    [Google Scholar]
  81. 81. 
    Amitai G, Sorek R. 2017. Intracellular signaling in CRISPR-Cas defense. Science 357:6351550–51
    [Google Scholar]
  82. 82. 
    Athukoralage JS, McMahon S, Zhang C, Grüschow S, Graham S et al. 2020. An anti-CRISPR viral ring nuclease subverts type III CRISPR immunity. Nature 577:572–75
    [Google Scholar]
  83. 83. 
    Athukoralage JS, Graham S, Grüschow S, Rouillon C, White MF 2019. A type III CRISPR ancillary ribonuclease degrades its cyclic oligoadenylate activator. J. Mol. Biol. 431:152894–99
    [Google Scholar]
  84. 84. 
    Meeske AJ, Nakandakari-Higa S, Marraffini LA 2019. Cas13-induced cellular dormancy prevents the rise of CRISPR-resistant bacteriophage. Nature 570:7760241–45
    [Google Scholar]
  85. 85. 
    Mendoza SD, Bondy-Denomy J. 2019. Cas13 helps bacteria play dead when the enemy strikes. Cell Host Microbe 26:11–2
    [Google Scholar]
  86. 86. 
    Labrie S, Samson J, Moineau S 2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8:317–27
    [Google Scholar]
  87. 87. 
    Dedrick RM, Jacobs-Sera D, Guerrero Bustamante CA, Garlena RA, Mavrich TN 2017. Prophage-mediated defense against viral attack and viral counter-defense. Nat. Microbiol. 2:16251
    [Google Scholar]
  88. 88. 
    Gentile GM, Wetzel KS, Dedrick RM, Montgomery MT, Garlena RA et al. 2019. More evidence of collusion: a new prophage-mediated viral defense system encoded by mycobacteriophage Sbash. mBio 10:e00196-19
    [Google Scholar]
  89. 89. 
    Montgomery MT, Guerrero Bustamante CA, Dedrick RM, Jacobs-Sera D, Hatfull GF 2019. Yet more evidence of collusion: a new viral defense system encoded by Gordonia phage CarolAnn. mBio 10:e02417-18
    [Google Scholar]
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