Conditional activation of toxin-antitoxin systems: Postsegregational killing and beyond

Microbiology Spectrum

Volumn 2, Issue 5, 2014, Pages

  Hernández Arriaga, Ana María ^a   Chan, Wai Ting ^a   Espinosa, Manuel ^a   Díaz Orejas, Ramón ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

TOXIN;

ANTAGONISTS AND INHIBITORS; ARCHAEON; BACTERIUM; CELL DIVISION; EXTRACHROMOSOMAL INHERITANCE; GENETICS; METABOLISM; MICROBIAL VIABILITY; PLASMID; TRANSPORT AT THE CELLULAR LEVEL;

ARCHAEA; BACTERIA; BIOLOGICAL TRANSPORT; CELL DIVISION; EXTRACHROMOSOMAL INHERITANCE; MICROBIAL VIABILITY; PLASMIDS; TOXINS, BIOLOGICAL;

EID: 84958811591     PISSN: None     EISSN: 21650497     Source Type: Journal    
DOI: 10.1128/microbiolspec.PLAS-0009-2013     Document Type: Article

References (126)

1. Gerdes K, Rasmussen PB, Molin S. 1986. Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. Proc Natl Acad Sci USA 83:3116-3120.
2. Jaffe A, Ogura T, Hiraga S. 1985. Effects of the ccd function of the F plasmid on bacterial growth. J Bacteriol 163:841-849.
3. Ogura T, Hiraga S. 1983. Mini-F plasmid genes that couple host cell division to plasmid proliferation. Proc Natl Acad Sci USA 80:4784-4788.
4. Pandey DP, Gerdes K. 2005. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res 33:966-976.
5. Van Melderen L, Saavedra De Bast M. 2009. Bacterial toxin-antitoxin systems: more than selfish entities? PLoS Genet 5:1-6.
6. Makarova KS, Wolf YI, Koonin EV. 2013. Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res 41:4360-4377.
7. Moller-Jensen J, Franch T, Gerdes K. 2001. Temporal translational control by a metastable RNA structure. J Biol Chem 276:35707-35713.
8. Brzozowska I, Zielenkiewicz U. 2013. Regulation of toxin-antitoxin systems by proteolysis. Plasmid 70:33-41.
9. Hayes F, Van Melderen L. 2011. Toxins-antitoxins: diversity, evolution and function. Crit Rev Biochem Mol Biol 46:386-408.
10. Masuda H, Tan Q, Awano N, Wu KP, Inouye M. 2012. YeeU enhances the bundling of cytoskeletal polymers of MreB and FtsZ, antagonizing the CbtA (YeeV) toxicity in Escherichia coli. Mol Microbiol 84:979-989.
11. Wang X, Lord DM, Cheng HY, Osbourne DO, Hong SH, Sanchez-Torres V, Quiroga C, Zheng K, Herrmann T, Peti W, Benedik MJ, Page R, Wood TK. 2012. A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS. Nat Chem Biol 8: 855-861.
12. Leplae R, Geeraerts D, Hallez R, Guglielmini J, Dreze 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 39:5513-5525.
13. Satwika D, Klassen R, Meinhardt F. 2012. Anticodon nuclease encoding virus-like elements in yeast. Appl Microbiol Biotechnol 96:345-356.
14. de la Cueva-Mendez G, Mills AD, Clay-Farrace L, Diaz-Orejas R, Laskey RA. 2003. Regulatable killing of eukaryotic cells by the prokaryotic proteins Kid and Kis. EMBO J 22:246-251.
15. Slanchev K, Stebler J, de la Cueva-Mendez G, Raz E. 2005. Development without germ cells: the role of the germ line in zebrafish sex differentiation. Proc Natl Acad Sci USA 102:4074-4079.
16. Gerdes K. 2012. In Gerdes K (ed), Prokaryotic Toxin-Antitoxins, 1st ed. Springer, Heidelberg, Germany.
17. Gerdes K, Christensen SK, Lobner-Olesen A. 2005. Prokaryotic toxinantitoxin stress response loci. Nat Rev 3:371-382.
18. CouturierM, Bahassiel M, Van Melderen L. 1998. Bacterial death by DNA gyrase poisoning. Trends Microbiol 6:269-275.
19. Buts L, Lah J, Dao-Thi MH, Wyns L, Loris R. 2005. Toxin-antitoxin modules as bacterial metabolic stress managers. Trends Biochem Sci 30: 672-679.
20. Condon C. 2006. Shutdown decay of mRNA. Mol Microbiol 61: 573-583.
21. Diago-Navarro E, Hernandez-Arriaga AM, Lopez-Villarejo J, Munoz-Gomez AJ, Kamphuis MB, Boelens R, Lemonnier M, Diaz-Orejas R. 2010. parD toxin-antitoxin system of plasmid R1-basic contributions, biotechnological applications and relationships with closely-related toxinantitoxin systems. FEBS J 277:3097-3117.
22. Chan WT, Moreno-Córdoba I, Yeo CC, Espinosa M. 2012. Toxinantitoxin genes of the gram-positive pathogen Streptococcus pneumoniae: so few and yet so many. Microbiol Mol Biol Rev 76:773-791.
23. Yamaguchi Y, Park JH, Inouye M. 2011. Toxin-antitoxin systems in bacteria and archaea. Annu Rev Genet 45:61-79.
24. Engelberg-Kulka H, Amitai S, Kolodkin-Gal I, Hazan R. 2006. Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet 2:e135. doi: 10.1371/journal.pgen.0020135.
25. Bernard P, Couturier M. 1992. Cell killing by the F plasmid CcdB protein involves poisoning of DNA-topoisomerase II complexes. J Mol Biol 226:735-745.
26. Miki T, Park JA, Nagao K, Murayama N, Horiuchi T. 1992. Control of segregation of chromosomal DNA by sex factor F in Escherichia coli. Mutants of DNA gyrase subunit A suppress letD (ccdB) product growth inhibition. J Mol Biol 225:39-52.
27. Bernard P, Kezdy KE, Van Melderen L, Steyaert J, Wyns L, Pato ML, Higgins PN, Couturier M. 1993. The F plasmid CcdB protein induces efficient ATP-dependentDNAcleavage by gyrase. J Mol Biol 234:534-541.
28. Bernard P, Couturier M. 1991. The 41 carboxy-terminal residues of the miniF plasmid CcdA protein are sufficient to antagonize the killer activity of the CcdB protein. Mol Gen Genet 226:297-304.
29. Madl T, Van Melderen L, Mine N, Respondek M, Oberer M, Keller W, Khatai L, Zangger K. 2006. Structural basis for nucleic acid and toxin recognition of the bacterial antitoxin CcdA. J Mol Biol 364:170-185.
30. Maki S, Takiguchi S, Horiuchi T, Sekimizu K, Miki T. 1996. Partner switching mechanisms in inactivation and rejuvenation of Escherichia coli DNA gyrase by F plasmid proteins LetD (CcdB) and LetA (CcdA). J Mol Biol 256:473-482.
31. Bahassi EM, O'Dea MH, Allali N, Messens J, Gellert M, Couturier M. 1999. Interactions of CcdB with DNA gyrase. Inactivation of Gyra, poisoning of the gyrase-DNA complex, and the antidote action of CcdA. J Biol Chem 274:10936-10944.
32. Dao-Thi MH, Charlier D, Loris R, Maes D, Messens J, Wyns L, Backmann J. 2002. Intricate interactions within the ccd plasmid addiction system. J Biol Chem 277:3733-3742.
33. De Jonge N, Garcia-Pino A, Buts L, Haesaerts S, Charlier D, Zangger K, Wyns L, De Greve H, Loris R. 2009. Rejuvenation of CcdB-poisoned gyrase by an intrinsically disordered protein domain. Mol Cell 35:154-163.
34. Van Melderen L, Bernard P, Couturier M. 1994. Lon-dependent proteolysis of CcdA is the key control for activation of CcdB in plasmidfree segregant bacteria. Mol Microbiol 11:1151-1157.
35. Van Melderen L, Thi MH, Lecchi P, Gottesman S, Couturier M, Maurizi MR. 1996. ATP-dependent degradation of CcdA by Lon protease. Effects of secondary structure and heterologous subunit interactions. J Biol Chem 271:27730-27738.
36. Gerdes K, Gultyaev AP, Franch T, Pedersen K, Mikkelsen ND. 1997. Antisense RNA-regulated programmed cell death. Annu Rev Genet 31: 1-31.
37. Gerdes K, Wagner EG. 2007. RNA antitoxins. Currt Opin Microbiol 10:117-124.
38. Weaver K. 2013. TypeI toxin-antitoxin loci: hok/sok and fst.9-26. In Gerdes K (ed), Prokariotic Toxin-Antitoxins, 21st ed. Springer, Heidelberg, Germany.
39. Bravo A, de Torrontegui G, Diaz R. 1987. Identification of components of a new stability system of plasmid R1, ParD, that is close to the origin of replication of this plasmid. Mol Gen Genet 210:101-110.
40. Tsuchimoto S, Ohtsubo H, Ohtsubo E. 1988. Two genes, pemK and pemI, responsible for stable maintenance of resistance plasmid R100. J Bacteriol 170:1461-1466.
41. Bravo A, Ortega S, de Torrontegui G, Diaz R. 1988. Killing of Escherichia coli cells modulated by components of the stability system ParD of plasmid R1. Mol Gen Genet 215:146-151.
42. Jensen RB, Grohmann E, Schwab H, Diaz-Orejas R, Gerdes K. 1995. Comparison of ccd of F, parDE of RP4, and parD of R1 using a novel conditional replication control system of plasmid R1. Mol Microbiol 17:211-220.
43. Munoz-Gomez AJ, Lemonnier M, Santos-Sierra S, Berzal-Herranz A, Diaz-Orejas R. 2005. RNase/anti-RNase activities of the bacterial parD toxin-antitoxin system. J Bacteriol 187:3151-3157.
44. Zhang J, Zhang Y, Zhu L, Suzuki M, Inouye M. 2004. Interference of mRNA function by sequence-specific endoribonuclease PemK. J Biol Chem 279:20678-20684.
45. Santos-Sierra S, Pardo-Abarrio C, Giraldo R, Diaz-Orejas R. 2002. Genetic identification of two functional regions in the antitoxin of the parD killer system of plasmid R1. FEMS Microbiol Lett 206:115-119.
46. Kamphuis MB, Monti MC, van den Heuvel RH, Santos-Sierra S, Folkers GE, Lemonnier M, Diaz-Orejas R, Heck AJ, Boelens R. 2007. Interactions between the toxin Kid of the bacterial parD system and the antitoxins Kis and MazE. Proteins 67:219-231.
47. Ruiz-Echevarria MJ, Berzal-Herranz A, Gerdes K, Diaz-Orejas R. 1991. The kis and kid genes of the parD maintenance system of plasmid R1 form an operon that is autoregulated at the level of transcription by the co-ordinated action of the Kis and Kid proteins. Mol Microbiol 5:2685-2693.
48. Monti MC, Hernandez-Arriaga AM, Kamphuis MB, Lopez-Villarejo J, Heck AJ, Boelens R, Diaz-Orejas R, van den Heuvel RH. 2007. Interactions of Kid-Kis toxin-antitoxin complexes with the parD operatorpromoter region of plasmid R1 are piloted by the Kis antitoxin and tuned by the stoichiometry of Kid-Kis oligomers. Nucleic Acids Res 35:1737-1749.
49. Ruiz-Echevarria MJ, de la Cueva G, Diaz-Orejas R. 1995. Translational coupling and limited degradation of a polycistronic messenger modulate differential gene expression in the parD stability system of plasmid R1. Mol Gen Genet 248:599-609.
50. Diago-Navarro E, Hernandez-Arriaga AM, Kubik S, Konieczny I, Diaz-Orejas R. 2013. Cleavage of the antitoxin of the parD toxin-antitoxin system is determined by the ClpAP protease and is modulated by the relative ratio of the toxin and the antitoxin. Plasmid 70:78-85.
51. Roberts RC, Helinski DR. 1992. Definition of a minimal plasmid stabilization system from the broad-host-range plasmid RK2. J Bacteriol 174:8119-8132.
52. Roberts RC, Strom AR, Helinski DR. 1994. The parDE operon of the broad-host-range plasmid RK2 specifies growth inhibition associated with plasmid loss. J Mol Biol 237:35-51.
53. Jiang Y, Pogliano J, Helinski DR, Konieczny I. 2002. ParE toxin encoded by the broad-host-range plasmid RK2 is an inhibitor of Escherichia coli gyrase. Mol Microbiol 44:971-979.
54. Davis TL, Helinski DR, Roberts RC. 1992. Transcription and autoregulation of the stabilizing functions of broad-host-range plasmid RK2 in Escherichia coli, Agrobacterium tumefaciens and Pseudomonas aeruginosa. Mol Microbiol 6:1981-1994.
55. Eberl L, Givskov M, Schwab H. 1992. The divergent promoters mediating transcription of the par locus of plasmid RP4 are subject to autoregulation. Mol Microbiol 6:1969-1979.
56. Roberts RC, Spangler C, Helinski DR. 1993. Characteristics and significance of DNA binding activity of plasmid stabilization protein ParD from the broad host-range plasmid RK2. J Biol Chem 268:27109-27117.
57. Johnson EP, Strom AR, Helinski DR. 1996. Plasmid RK2 toxin protein ParE: purification and interaction with the ParD antitoxin protein. J Bacteriol 178:1420-1429.
58. Oberer M, Zangger K, Gruber K, Keller W. 2007. The solution structure of ParD, the antidote of the ParDE toxin antitoxin module, provides the structural basis for DNA and toxin binding. Protein Sci 16:1676-1688.
59. Lehnherr H, Maguin E, Jafri S, Yarmolinsky MB. 1993. Plasmid addiction genes of bacteriophage P1: doc, which causes cell death on curing of prophage, and phd, which prevents host death when prophage is retained. J Mol Biol 233:414-428.
60. Makarova KS, Wolf YI, Koonin EV. 2009. Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol Direct 4:19. doi: 10.1186/1745-6150-4-19.
61. Liu M, Zhang Y, Inouye M, Woychik NA. 2008. Bacterial addiction module toxin Doc inhibits translation elongation through its association with the 30S ribosomal subunit. Proc Natl Acad Sci USA 105:5885-5890.
62. Hazan R, Sat B, Reches M, Engelberg-Kulka H. 2001. Postsegregational killing mediated by the P1 phage "addiction module" phd-doc requires the Escherichia coli programmed cell death system mazEF. J Bacteriol 183:2046-2050.
63. Magnuson R, Lehnherr H, Mukhopadhyay G, Yarmolinsky MB. 1996. Autoregulation of the plasmid addiction operon of bacteriophage P1. J Biol Chem 271:18705-18710.
64. Magnuson R, Yarmolinsky MB. 1998. Corepression of the P1 addiction operon by Phd and Doc. J Bacteriol 180:6342-6351.
65. Garcia-Pino A, Balasubramanian S, Wyns L, Gazit E, De Greve H, Magnuson RD, Charlier D, van Nuland NA, Loris R. 2010. Allostery and intrinsic disorder mediate transcription regulation by conditional cooperativity. Cell 142:101-111.
66. Lehnherr H, Yarmolinsky MB. 1995. Addiction protein Phd of plasmid prophage P1 is a substrate of the ClpXP serine protease of Escherichia coli. Proc Natl Acad Sci USA 92:3274-3277.
67. Engelberg-Kulka H, Reches M, Narasimhan S, Schoulaker-Schwarz R, Klemes Y, Aizenman E, Glaser G. 1998. rexB of bacteriophage lambda is an anti-cell death gene. Proc Natl Acad Sci USA 95:15481-15486.
68. Fineran PC, Blower TR, Foulds IJ, Humphreys DP, Lilley KS, Salmond GP. 2009. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc Natl Acad Sci USA 106:894-899.
69. Blower T, Fineran P, Johnson M, Toth I, Humphreys D, Salmond G. 2009. Mutagenesis and functional characterization of the RNA and protein components of the toxIN abortive infection and toxin-antitoxin locus of Erwinia. J Bacteriol 191:6029-6039.
70. Chopin MC, Chopin A, Bidnenko E. 2005. Phage abortive infection in lactococci: variations on a theme. Curr Opin Microbiol 8:473-479.
71. Blower TR, Pei XY, Short FL, Fineran PC, Humphreys DP, Luisi BF, Salmond GP. 2011. A processed noncoding RNA regulates an altruistic bacterial antiviral system. Nat Struct Mol Biol 18:185-190.
72. Short FL, Pei XY, Blower TR, Ong SL, Fineran PC, Luisi BF, Salmond GP. 2012. Selectivity and self-assembly in the control of a bacterial toxin by an antitoxic noncoding RNA pseudoknot. Proc Natl Acad Sci USA 110:E241-E249.
73. Nordstrom K. 2006. Plasmid R1-replication and its control. Plasmid 55:1-26.
74. Ruiz-Echevarria MJ, de la Torre MA, Diaz-Orejas R. 1995. A mutation that decreases the efficiency of plasmid R1 replication leads to the activation of parD, a killer stability system of the plasmid. FEMS Microbiol Lett 130:129-135.
75. Lopez-Villarejo J, Diago-Navarro E, Hernandez-Arriaga AM, Diaz-Orejas R. 2012. Kis antitoxin couples plasmid R1 replication and parD (kis, kid) maintenance modules. Plasmid 67:118-127.
76. Pimentel B, Madine MA, de la Cueva-Mendez G. 2005. Kid cleaves specific mRNAs at UUACU sites to rescue the copy number of plasmid R1. EMBO J 24:3459-3469.
77. Lewis K. 2010. Persister cells. Annu Rev Microbiol 64:357-372.
78. Cooper TF, Heinemann JA. 2000. Postsegregational killing does not increase plasmid stability but acts to mediate the exclusion of competing plasmids. Proc Natl Acad Sci USA 97:12643-12648.
79. Cooper TF, Paixão T, Heinemann JA. 2010. Within-host competition selects for plasmid-encoded toxin-antitoxin systems. Proc Biol Sci 22:3149-3155.
80. Naito T, Kusano K, Kobayashi I. 1995. Selfish behavior of restrictionmodification systems. Science (New York, NY) 267:897-899.
81. Naito Y, Naito T, Kobayashi I. 1998. Selfish restriction modification genes: resistance of a resident R/M plasmid to displacement by an incompatible plasmid mediated by host killing. Biol Chem 379:429-436.
82. Saavedra De Bast M, Mine N, Van Melderen L. 2008. Chromosomal toxin-antitoxin systems may act as antiaddiction modules. J Bacteriol 190: 4603-4609.
83. Santos-Sierra S, Giraldo R, Diaz-Orejas R. 1997. Functional interactions between homologous conditional killer systems of plasmid and chromosomal origin. FEMS Microbiol Lett 152:51-56.
84. Hargreaves D, Santos-Sierra S, Giraldo R, Sabariegos-Jareno R, de la Cueva-Mendez G, Boelens R, Diaz-Orejas R, Rafferty JB. 2002. Structural and functional analysis of the kid toxin protein from E. coli plasmid R1. Structure 10:1425-1433.
85. Smith AB, Lopez-Villarejo J, Diago-Navarro E, Mitchenall LA, Barendregt A, Heck AJ, Lemonnier M, Maxwell A, Diaz-Orejas R. 2012. A common origin for the bacterial toxin-antitoxin systems parD and ccd, suggested by analyses of toxin/target and toxin/antitoxin interactions. PloS One 7:e46499. doi: 10.1371/journal.pone.0046499.
86. Francuski D, Saenger W. 2009. Crystal structure of the antitoxin-toxin protein complex RelB-RelE from Methanococcus jannaschii. J Mol Biol 393:898-908.
87. Pedersen K, Zavialov AV, Pavlov MY, Elf J, Gerdes K, Ehrenberg M. 2003. The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell 112:131-140.
88. Zhang Y, Inouye M. 2009. The inhibitory mechanism of protein synthesis by YoeB, an Escherichia coli toxin. J Biol Chem 284:6627-6638.
89. Makarova KS, Wolf YI, Snir S, Koonin EV. 2011. Defense islands in bacterial and archaeal genomes and prediction of novel defense systems. J Bacteriol 193:6039-6056.
90. Pandey DP, Gerdes K. 2005. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res 33:966-976.
91. Wozniak RA, Waldor MK. 2009. A toxin-antitoxin system promotes the maintenance of an integrative conjugative element. PLoS Genet 5: e1000439. doi: 10.1371/journal.pgen.1000439.
92. Rowe-Magnus DA, Guerout AM, Biskri L, Bouige P, Mazel D. 2003. Comparative analysis of superintegrons: engineering extensive genetic diversity in the Vibrionaceae. Genome Res 13:428-442.
93. Szekeres S, Dauti M, Wilde C, Mazel D, Rowe-Magnus DA. 2007. Chromosomal toxin-antitoxin loci can diminish large-scale genome reductions in the absence of selection. Mol. Microbiol 63:1588-1605.
94. Christensen KS, Maenhauf-Michel G, Mine N, Gothesman S, Gerdes K, Van Melderen L. 2004. Overproduction of the Lon protease triggers inhibition of translation in Escherichia coli: involvement of the yefM-yoeB toxin-antitoxin system. Mol Microbiol 51:1705-1717.
95. Yuan J, Yamaichi Y, Waldor MK. 2011. The three vibrio cholerae chromosome II-encoded ParE toxins degrade chromosome I following loss of chromosome II. J Bacteriol 193:611-619.
96. Egan ES, Fogel MA, Waldor MK. 2005. Divided genomes: negotiating the cell cycle in prokaryotes with multiple chromosomes. Mol Microbiol 56:1129-1138.
97. Srivastava P, Chattoraj DK. 2007. Selective chromosome amplification in Vibrio cholerae. Mol Microbiol 66:1016-1028.
98. Brown JS, Gilliland SM, Spratt BG, Holden DW. 2004. A locus contained within a variable region of pneumococcal pathogenicity island 1 contributes to virulence in mice. Infect Immun 72:1587-1593.
99. Khoo SK, Loll B, Chan WT, Shoeman RL, Ngoo L, Yeo CC, Meinhart A. 2007. Molecular and structural characterization of the PezAT chromosomal toxin-antitoxin system of the human pathogen Streptococcus pneumoniae. J Biol Chem 282:19606-19618.
100. Dordet-Frisoni E, Marenda MS, Sagne E, Nouvel LX, Blanchard A, Tardy F, Sirand-Pugnet P, Baranowski E, Citti C. 2013. ICEA of Mycoplasma agalactiae: a new family of self-transmissible integrative element that confers conjugative properties to the recipient strain. Mol Microbiol 89:1226-1239.
101. Christensen SK, Pedersen K, Hansen FG, Gerdes K. 2003. Toxinantitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA. J Mol Biol 332:809-819.
102. Moyed HS, Bertrand KP. 1983. hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J Bacteriol 155:768-775.
103. Kim Y, Wang X, Ma Q, Zhang XS, Wood TK. 2009. Toxinantitoxin systems in Escherichia coli influence biofilm formation through YjgK (TabA) and fimbriae. J Bacteriol 191:1258-1267.
104. Chan WT, Nieto C, Harikrishna JA, Khoo SK, Yasmin Othman R, Espinosa M, Yeo CC. 2011. Genetic regulation of the yefM-yoeBSpn toxinantitoxin locus of Streptococcus pneumoniae. J Bacteriol 193:4612-4625.
105. Knutsen E, Johnsborg O, Quentin Y, Claverys JP, Havarstein LS. 2006. BOX elements modulate gene expression in Streptococcus pneumoniae: impact on the fine-tuning of competence development. J Bacteriol 188:8307-8312.
106. Petersen J, Frank O, Göker M, Pradella S. 2013. Extrachromosomal, extraordinary and essential: the plasmids of the Roseobacter clade. Appl Microbiol Biotechnol 97:2805-2815.
107. González V, Santamaría RI, Bustos P, Hernández-González I, Medrano-Soto A, Moreno-Hagelsieb G, Janga SC, Ramírez MA, Jiménez-Jacinto V, Collado-Vides J, Dávila G. 2006. The partitioned Rhizobium etli genome: Genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci USA 103:3834-3839.
108. Dempsey LA, Dubnau D. 1989. Identification of plasmid and Bacillus subtilis chromosomal recombination sites used for pE194 integration. J Bacteriol 171:2856-2865.
109. Hahn J, Dubnau D. 1985. Analysis of plasmid deletional instability in Bacillus subtilis. J Bacteriol 162:1014-1023.
110. Baquero F. 2004. From pieces to patterns: evolutionary engineering in bacterial pathogens. Nat Rev Microbiol 2:510-518.
111. Baquero F. 2009. Environmental stress and evolvability in microbial systems. Clin Microbiol Infect 15:5-10.
112. Camacho EM, Serna A, Madrid C, Marqués S, Fernández R, de la Cruz F, Juárez A, Casadesús J. 2005. Regulation of finP transcription by DNA adenine methylation in the virulence plasmid of Salmonella enterica. J Bacteriol 187:5691-5699.
113. Harr B, Schlötterer C. 2006. Gene expression analysis indicates extensive genotype-specific crosstalk between the conjugative F-plasmid and the E. coli chromosome. BMC Microbiol 6:80. doi:10.1186/1471-2180-6-80.
114. Maida I, Fondi M, Papaleo MC, Perrin E, Fani R. 2011. The gene flow between plasmids and chromosomes: insights from bioinformatics analyses. Open Appl Informatics J 5:62-76.
115. Kasari V, Mets T, Tenson T, Kaldalu N. 2013. Transcriptional crossactivation between toxin-antitoxin systems of Escherichia coli. BMC Microbiol 13:45. doi: 10.1186/1471-2180-13-45.
116. Winther KS, Gerdes K. 2009. Ectopic production of VapCs from Enterobacteria inhibits translation and trans-activates YoeB mRNA interferase. Mol Microbiol 72:918-930.
117. Wang X, Lord DM, Hong SH, Peti W, Benedik MJ, Page R, Wood TK. 2013. Type II toxin/antitoxin MqsR/MqsA controls type V toxin/antitoxin GhoT/GhoS. Environ Microbiol 15:1734-1744.
118. Wang X, Kim Y, Hong SH, Ma Q, Brown BL, Pu M, Tarone AM, Benedik M, Peti W, Page R, Wood TK. 2011. Antitoxin MqsA helps mediate the bacterial general stress response. Nat Chem Biol 7:359-366.
119. Maisonneuve E, Shakespeare LJ, Jørgensen MG, Gerdes K. 2011. Bacterial persistence by RNA endonucleases. Proc Natl Acad Sci USA 108:13206-13211.
120. 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: e1000767. doi: 10.1371/journal.pgen.1000767.
121. Wilbaux M, Mine N, Guerout AM, Mazel D, Van Melderen L. 2007. Functional interactions between coexisting toxin-antitoxin systems of the ccd family in Escherichia coli O157:H7. J Bacteriol 189:2712-2719.
122. Wilbaux M, Mine N, Guerout A-M, Mazel D, Van Melderen L. 2007. Functional interactions between coexisting toxin-antitoxin systems of the ccd family in Escherichia coli O157:H7. J Bacteriol 189:2712-2719.
123. Gronlund H, Gerdes K. 1999. Toxin-antitoxin systems homologous with relBE of Escherichia coli plasmid P307 are ubiquitous in prokaryotes. J Mol Biol 285:1401-1415.
124. Yuan J, Sterckx Y, Mitchenall LA, Maxwell A, Loris R, Waldor MK. 2010. Vibrio cholerae ParE2 poisons DNA gyrase via a mechanism distinct from other gyrase inhibitors. J Biol Chem 285:40397-40408.
125. Tripathi A, Dewan PC, Barua B, Varadarajan R. 2012. Additional role for the ccd operon of F-plasmid as a transmissible persistence factor. Proc Natl Acad Sci USA 109:12497-12502.
126. Volante A, Soberón NE, Ayora S, Alonso JC. The interplay between different stability systems contributes to faithful segregation: Streptococcus pyogenes pSM19035 as a model. In Tolmasky ME, Alonso JC, Plasmids: Biology and Impact in Biotechnology and Discovery. ASM Press, Washington, DC, in press.