Published online 17 February 2005
Article |
Toxinantitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes
Department of Biochemistry and Molecular Biology, University of Southern Denmark DK-5230 Odense M, Denmark
*To whom correspondence should be addressed. Tel: +45 6550 2413; Fax: +45 6550 2769; Email: kgerdes{at}bmb.sdu.dk
Received October 29, 2004. Revised December 30, 2004. Accepted December 30, 2004.
Prokaryotic chromosomes code for toxinantitoxin (TA) loci, often in multiple copies. In E.coli, experimental evidence indicates that TA loci are stress-response elements that help cells survive unfavorable growth conditions. The first gene in a TA operon codes for an antitoxin that combines with and neutralizes a regulatory toxin, encoded by the second gene. RelE and MazF toxins are regulators of translation that cleave mRNA and function, in interplay with tmRNA, in quality control of gene expression. Here, we present the results from an exhaustive search for TA loci in 126 completely sequenced prokaryotic genomes (16 archaea and 110 bacteria). We identified 671 TA loci belonging to the seven known TA gene families. Surprisingly, obligate intracellular organisms were devoid of TA loci, whereas free-living slowly growing prokaryotes had particularly many (38 in Mycobacterium tuberculosis and 43 in Nitrosomonas europaea). In many cases, TA loci were clustered and closely linked to mobile genetic elements. In the most extreme of these cases, all 13 TA loci of Vibrio cholerae were bona fide integron elements located in the V.cholerae mega-integron. These observations strongly suggest that TA loci are mobile cassettes that move frequently within and between chromosomes and also lend support to the hypothesis that TA loci function as stress-response elements beneficial to free-living prokaryotes.
![]()
CiteULike
Connotea
Del.icio.us What's this?
This article has been cited by other articles:
![]() |
D. A. Walsh, E. Zaikova, C. G. Howes, Y. C. Song, J. J. Wright, S. G. Tringe, P. D. Tortell, and S. J. Hallam Metagenome of a Versatile Chemolithoautotroph from Expanding Oceanic Dead Zones Science, October 23, 2009; 326(5952): 578 - 582. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Yamaguchi, J.-H. Park, and M. Inouye MqsR, a Crucial Regulator for Quorum Sensing and Biofilm Formation, Is a GCU-specific mRNA Interferase in Escherichia coli J. Biol. Chem., October 16, 2009; 284(42): 28746 - 28753. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Baik, K. Inoue, M. Ouyang, and M. Inouye Significant Bias against the ACA Triplet in the tmRNA Sequence of Escherichia coli K-12 J. Bacteriol., October 1, 2009; 191(19): 6157 - 6166. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Yoshizumi, Y. Zhang, Y. Yamaguchi, L. Chen, B. N. Kreiswirth, and M. Inouye Staphylococcus aureus YoeB Homologues Inhibit Translation Initiation J. Bacteriol., September 15, 2009; 191(18): 5868 - 5872. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. M. Hurley and N. A. Woychik Bacterial Toxin HigB Associates with Ribosomes and Mediates Translation-dependent mRNA Cleavage at A-rich Sites J. Biol. Chem., July 10, 2009; 284(28): 18605 - 18613. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. d. l. P. Santangelo, L. Klepp, J. Nunez-Garcia, F. C. Blanco, M. Soria, M. d. C. Garcia-Pelayo, M. V. Bianco, A. A. Cataldi, P. Golby, M. Jackson, et al. Mce3R, a TetR-type transcriptional repressor, controls the expression of a regulon involved in lipid metabolism in Mycobacterium tuberculosis Microbiology, July 1, 2009; 155(7): 2245 - 2255. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. L. Reno, N. L. Held, C. J. Fields, P. V. Burke, and R. J. Whitaker Biogeography of the Sulfolobus islandicus pan-genome PNAS, May 26, 2009; 106(21): 8605 - 8610. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. Kolodkin-Gal and H. Engelberg-Kulka The Stationary-Phase Sigma Factor {sigma}S Is Responsible for the Resistance of Escherichia coli Stationary-Phase Cells to mazEF-Mediated Cell Death J. Bacteriol., May 1, 2009; 191(9): 3177 - 3182. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. P. Donegan and A. L. Cheung Regulation of the mazEF Toxin-Antitoxin Module in Staphylococcus aureus and Its Impact on sigB Expression J. Bacteriol., April 15, 2009; 191(8): 2795 - 2805. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Provvedi, F. Boldrin, F. Falciani, G. Palu, and R. Manganelli Global transcriptional response to vancomycin in Mycobacterium tuberculosis Microbiology, April 1, 2009; 155(4): 1093 - 1102. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Mine, J. Guglielmini, M. Wilbaux, and L. Van Melderen The Decay of the Chromosomally Encoded ccdO157 Toxin-Antitoxin System in the Escherichia coli Species Genetics, April 1, 2009; 181(4): 1557 - 1566. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. B. Korch, H. Contreras, and J. E. Clark-Curtiss Three Mycobacterium tuberculosis Rel Toxin-Antitoxin Modules Inhibit Mycobacterial Growth and Are Expressed in Infected Human Macrophages J. Bacteriol., March 1, 2009; 191(5): 1618 - 1630. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. G. Jorgensen, D. P. Pandey, M. Jaskolska, and K. Gerdes HicA of Escherichia coli Defines a Novel Family of Translation-Independent mRNA Interferases in Bacteria and Archaea J. Bacteriol., February 15, 2009; 191(4): 1191 - 1199. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. E. S. Bailey and F. Hayes Influence of Operator Site Geometry on Transcriptional Control by the YefM-YoeB Toxin-Antitoxin Complex J. Bacteriol., February 1, 2009; 191(3): 762 - 772. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Miallau, M. Faller, J. Chiang, M. Arbing, F. Guo, D. Cascio, and D. Eisenberg Structure and Proposed Activity of a Member of the VapBC Family of Toxin-Antitoxin Systems: VapBC-5 FROM MYCOBACTERIUM TUBERCULOSIS J. Biol. Chem., January 2, 2009; 284(1): 276 - 283. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Manos, J. Arthur, B. Rose, P. Tingpej, C. Fung, M. Curtis, J. S. Webb, H. Hu, S. Kjelleberg, M. D. Gorrell, et al. Transcriptome analyses and biofilm-forming characteristics of a clonal Pseudomonas aeruginosa from the cystic fibrosis lung J. Med. Microbiol., December 1, 2008; 57(12): 1454 - 1465. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Garcia-Pino, M. Christensen-Dalsgaard, L. Wyns, M. Yarmolinsky, R. D. Magnuson, K. Gerdes, and R. Loris Doc of Prophage P1 Is Inhibited by Its Antitoxin Partner Phd through Fold Complementation J. Biol. Chem., November 7, 2008; 283(45): 30821 - 30827. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Christensen-Dalsgaard and K. Gerdes Translation affects YoeB and MazF messenger RNA interferase activities by different mechanisms Nucleic Acids Res., November 1, 2008; 36(20): 6472 - 6481. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Saavedra De Bast, N. Mine, and L. Van Melderen Chromosomal Toxin-Antitoxin Systems May Act as Antiaddiction Modules J. Bacteriol., July 1, 2008; 190(13): 4603 - 4609. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Savvi, D. F. Warner, B. D. Kana, J. D. McKinney, V. Mizrahi, and S. S. Dawes Functional Characterization of a Vitamin B12-Dependent Methylmalonyl Pathway in Mycobacterium tuberculosis: Implications for Propionate Metabolism during Growth on Fatty Acids J. Bacteriol., June 1, 2008; 190(11): 3886 - 3895. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. Kolodkin-Gal and H. Engelberg-Kulka The Extracellular Death Factor: Physiological and Genetic Factors Influencing Its Production and Response in Escherichia coli J. Bacteriol., May 1, 2008; 190(9): 3169 - 3175. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Liu, Y. Zhang, M. Inouye, and N. A. Woychik Bacterial addiction module toxin Doc inhibits translation elongation through its association with the 30S ribosomal subunit PNAS, April 15, 2008; 105(15): 5885 - 5890. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. C. Rice and K. W. Bayles Molecular Control of Bacterial Death and Lysis Microbiol. Mol. Biol. Rev., March 1, 2008; 72(1): 85 - 109. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. C. Hett and E. J. Rubin Bacterial Growth and Cell Division: a Mycobacterial Perspective Microbiol. Mol. Biol. Rev., March 1, 2008; 72(1): 126 - 156. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. Kolodkin-Gal, R. Hazan, A. Gaathon, S. Carmeli, and H. Engelberg-Kulka A Linear Pentapeptide Is a Quorum-Sensing Factor Required for mazEF-Mediated Cell Death in Escherichia coli Science, October 26, 2007; 318(5850): 652 - 655. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Golby, K. A. Hatch, J. Bacon, R. Cooney, P. Riley, J. Allnutt, J. Hinds, J. Nunez, P. D. Marsh, R. G. Hewinson, et al. Comparative transcriptomics reveals key gene expression differences between the human and bovine pathogens of the Mycobacterium tuberculosis complex Microbiology, October 1, 2007; 153(10): 3323 - 3336. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Villain-Guillot, M. Gualtieri, L. Bastide, and J.-P. Leonetti In Vitro Activities of Different Inhibitors of Bacterial Transcription against Staphylococcus epidermidis Biofilm Antimicrob. Agents Chemother., September 1, 2007; 51(9): 3117 - 3121. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. Tsilibaris, G. Maenhaut-Michel, N. Mine, and L. Van Melderen What Is the Benefit to Escherichia coli of Having Multiple Toxin-Antitoxin Systems in Its Genome? J. Bacteriol., September 1, 2007; 189(17): 6101 - 6108. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. D. Magnuson Hypothetical Functions of Toxin-Antitoxin Systems J. Bacteriol., September 1, 2007; 189(17): 6089 - 6092. [Full Text] [PDF] |
||||
![]() |
J. Sjoholm, P. Oliveira, and P. Lindblad Transcription and Regulation of the Bidirectional Hydrogenase in the Cyanobacterium Nostoc sp. Strain PCC 7120 Appl. Envir. Microbiol., September 1, 2007; 73(17): 5435 - 5446. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. A. Daines, M. H. Wu, and S. Y. Yuan VapC-1 of Nontypeable Haemophilus influenzae Is a Ribonuclease J. Bacteriol., July 15, 2007; 189(14): 5041 - 5048. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. K. Khoo, B. Loll, W. T. Chan, R. L. Shoeman, L. Ngoo, C. C. Yeo, and A. Meinhart Molecular and Structural Characterization of the PezAT Chromosomal Toxin-Antitoxin System of the Human Pathogen Streptococcus pneumoniae J. Biol. Chem., July 6, 2007; 282(27): 19606 - 19618. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. O. Gvakharia, E. A. Permina, M. S. Gelfand, P. J. Bottomley, L. A. Sayavedra-Soto, and D. J. Arp Global Transcriptional Response of Nitrosomonas europaea to Chloroform and Chloromethane Appl. Envir. Microbiol., May 15, 2007; 73(10): 3440 - 3445. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Wilbaux, N. Mine, A.-M. Guerout, D. Mazel, and L. Van Melderen Functional Interactions between Coexisting Toxin-Antitoxin Systems of the ccd Family in Escherichia coli O157:H7 J. Bacteriol., April 1, 2007; 189(7): 2712 - 2719. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Dziewit, M. Jazurek, L. Drewniak, J. Baj, and D. Bartosik The SXT Conjugative Element and Linear Prophage N15 Encode Toxin-Antitoxin-Stabilizing Systems Homologous to the tad-ata Module of the Paracoccus aminophilus Plasmid pAMI2 J. Bacteriol., March 1, 2007; 189(5): 1983 - 1997. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Nieto, I. Cherny, S. K. Khoo, M. G. de Lacoba, W. T. Chan, C. C. Yeo, E. Gazit, and M. Espinosa The yefM-yoeB Toxin-Antitoxin Systems of Escherichia coli and Streptococcus pneumoniae: Functional and Structural Correlation J. Bacteriol., February 15, 2007; 189(4): 1266 - 1278. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. P. Budde, B. M. Davis, J. Yuan, and M. K. Waldor Characterization of a higBA Toxin-Antitoxin Locus in Vibrio cholerae J. Bacteriol., January 15, 2007; 189(2): 491 - 500. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Kedzierska, L.-Y. Lian, and F. Hayes Toxin-antitoxin regulation: bimodal interaction of YefM-YoeB with paired DNA palindromes exerts transcriptional autorepression Nucleic Acids Res., January 12, 2007; 35(1): 325 - 339. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Yamaichi, M. A. Fogel, and M. K. Waldor par genes and the pathology of chromosome loss in Vibrio cholerae PNAS, January 9, 2007; 104(2): 630 - 635. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. M. Moritz and P. J. Hergenrother Toxin-antitoxin systems are ubiquitous and plasmid-encoded in vancomycin-resistant enterococci PNAS, January 2, 2007; 104(1): 311 - 316. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. F. Correia, A. D'Onofrio, T. Rejtar, L. Li, B. L. Karger, K. Makarova, E. V. Koonin, and K. Lewis Kinase Activity of Overexpressed HipA Is Required for Growth Arrest and Multidrug Tolerance in Escherichia coli J. Bacteriol., December 15, 2006; 188(24): 8360 - 8367. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Mattison, J. S. Wilbur, M. So, and R. G. Brennan Structure of FitAB from Neisseria gonorrhoeae Bound to DNA Reveals a Tetramer of Toxin-Antitoxin Heterodimers Containing Pin Domains and Ribbon-Helix-Helix Motifs J. Biol. Chem., December 8, 2006; 281(49): 37942 - 37951. [Abstract] [Full Text] [PDF] |
||||
![]() |
O. R. Faridani, A. Nikravesh, D. P. Pandey, K. Gerdes, and L. Good Competitive inhibition of natural antisense Sok-RNA interactions activates Hok-mediated cell killing in Escherichia coli Nucleic Acids Res., November 6, 2006; 34(20): 5915 - 5922. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. S. Makarova, N. V. Grishin, and E. V. Koonin The HicAB cassette, a putative novel, RNA-targeting toxin-antitoxin system in archaea and bacteria Bioinformatics, November 1, 2006; 22(21): 2581 - 2584. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Venkova-Canova, P. Srivastava, and D. K. Chattoraj Transcriptional inactivation of a regulatory site for replication of Vibrio cholerae chromosome II PNAS, August 8, 2006; 103(32): 12051 - 12056. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. S. Lioy, M. T. Martin, A. G. Camacho, R. Lurz, H. Antelmann, M. Hecker, E. Hitchin, Y. Ridge, J. M. Wells, and J. C. Alonso pSM19035-encoded {zeta} toxin induces stasis followed by death in a subpopulation of cells. Microbiology, August 1, 2006; 152(Pt 8): 2365 - 2379. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Zhu, Y. Zhang, J.-S. Teh, J. Zhang, N. Connell, H. Rubin, and M. Inouye Characterization of mRNA Interferases from Mycobacterium tuberculosis J. Biol. Chem., July 7, 2006; 281(27): 18638 - 18643. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. F. Warner and V. Mizrahi Tuberculosis Chemotherapy: the Influence of Bacillary Stress and Damage Response Pathways on Drug Efficacy Clin. Microbiol. Rev., July 1, 2006; 19(3): 558 - 570. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. B. Korch and T. M. Hill Ectopic Overexpression of Wild-Type and Mutant hipA Genes in Escherichia coli: Effects on Macromolecular Synthesis and Persister Formation J. Bacteriol., June 1, 2006; 188(11): 3826 - 3836. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Tachdjian and R. M. Kelly Dynamic Metabolic Adjustments and Genome Plasticity Are Implicated in the Heat Shock Response of the Extremely Thermoacidophilic Archaeon Sulfolobus solfataricus. J. Bacteriol., June 1, 2006; 188(12): 4553 - 4559. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. Kolodkin-Gal and H. Engelberg-Kulka Induction of Escherichia coli Chromosomal mazEF by Stressful Conditions Causes an Irreversible Loss of Viability J. Bacteriol., May 1, 2006; 188(9): 3420 - 3423. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Mochizuki, K. Yahara, I. Kobayashi, and Y. Iwasa Genetic Addiction: Selfish Gene's Strategy for Symbiosis in the Genome Genetics, February 1, 2006; 172(2): 1309 - 1323. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. R. Mey, E. E. Wyckoff, V. Kanukurthy, C. R. Fisher, and S. M. Payne Iron and Fur Regulation in Vibrio cholerae and the Role of Fur in Virulence Infect. Immun., December 1, 2005; 73(12): 8167 - 8178. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. M. Silvaggi, J. B. Perkins, and R. Losick Small Untranslated RNA Antitoxin in Bacillus subtilis J. Bacteriol., October 1, 2005; 187(19): 6641 - 6650. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Engelberg-Kulka, R. Hazan, and S. Amitai mazEF: a chromosomal toxin-antitoxin module that triggers programmed cell death in bacteria J. Cell Sci., October 1, 2005; 118(19): 4327 - 4332. [Abstract] [Full Text] [PDF] |
||||














