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PMID: 15718296 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes.

Nucleic acids research ·Vol. 33 ·No. 3 ·2005-00-00 ·Pages 966-76

Pandey DP, Gerdes K

Abstract

Prokaryotic chromosomes code for toxin-antitoxin (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.

MeSH Terms
Bacterial Toxins/classification,genetics Chromosome Mapping Enterobacteriaceae/genetics Genes, Archaeal Genes, Bacterial Integrons Interspersed Repetitive Sequences Phylogeny Toxins, Biological/classification,genetics Vibrio cholerae/genetics
Chemicals
Bacterial Toxins Toxins, Biological
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Pandey Deo Prakash
Department of Biochemistry and Molecular Biology, University of Southern Denmark DK-5230 Odense M, Denmark.
Gerdes Kenn
References (55)
55 references, click to expand
  1. The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site.
    Cell. 2003 Jan 10;112(1):131-40 PMID: 12526800
  2. Toxin-antitoxin systems homologous with relBE of Escherichia coli plasmid P307 are ubiquitous in prokaryotes.
    J Mol Biol. 1999 Jan 29;285(4):1401-15 PMID: 9917385
  3. The SsrA-SmpB system for protein tagging, directed degradation and ribosome rescue.
    Nat Struct Biol. 2000 Jun;7(6):449-55 PMID: 10881189
  4. Occurrence of mazEF-like antitoxin/toxin systems in bacteria.
    J Mol Microbiol Biotechnol. 1999 Nov;1(2):295-302 PMID: 10943559
  5. Evolution of prokaryotic gene order: genome rearrangements in closely related species.
    Trends Genet. 2001 Jan;17(1):10-3 PMID: 11163906
  6. Postsegregational killing mediated by the P1 phage "addiction module" phd-doc requires the Escherichia coli programmed cell death system mazEF.
    J Bacteriol. 2001 Mar;183(6):2046-50 PMID: 11222604
  7. Massive gene decay in the leprosy bacillus.
    Nature. 2001 Feb 22;409(6823):1007-11 PMID: 11234002
  8. Mechanisms of evolution in Rickettsia conorii and R. prowazekii.
    Science. 2001 Sep 14;293(5537):2093-8 PMID: 11557893
  9. Discovery and distribution of super-integrons among pseudomonads.
    Mol Microbiol. 2001 Nov;42(3):587-601 PMID: 11722728
  10. RelE, a global inhibitor of translation, is activated during nutritional stress.
    Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14328-33 PMID: 11717402
  11. ParE toxin encoded by the broad-host-range plasmid RK2 is an inhibitor of Escherichia coli gyrase.
    Mol Microbiol. 2002 May;44(4):971-9 PMID: 12010492
  12. 50 million years of genomic stasis in endosymbiotic bacteria.
    Science. 2002 Jun 28;296(5577):2376-9 PMID: 12089438
  13. Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins.
    Mol Microbiol. 2002 Jul;45(2):501-10 PMID: 12123459
  14. Toxin-antitoxin pairs in bacteria: killers or stress regulators?
    Cell. 2003 Jan 10;112(1):2-4 PMID: 12526786
  15. Axe-Txe, a broad-spectrum proteic toxin-antitoxin system specified by a multidrug-resistant, clinical isolate of Enterococcus faecium.
    Mol Microbiol. 2003 Mar;47(5):1419-32 PMID: 12603745
  16. Comparative analysis of superintegrons: engineering extensive genetic diversity in the Vibrionaceae.
    Genome Res. 2003 Mar;13(3):428-42 PMID: 12618374
  17. The Escherichia coli mazEF suicide module mediates thymineless death.
    J Bacteriol. 2003 Mar;185(6):1803-7 PMID: 12618443
  18. SsrA-mediated trans-translation plays a role in mRNA quality control by facilitating degradation of truncated mRNAs.
    RNA. 2003 Apr;9(4):408-18 PMID: 12649493
  19. Conditional senescence in bacteria: death of the immortals.
    Mol Microbiol. 2003 Apr;48(1):17-23 PMID: 12657042
  20. How introns influence and enhance eukaryotic gene expression.
    Trends Biochem Sci. 2003 Apr;28(4):215-20 PMID: 12713906
  21. Complete genome sequence of the Q-fever pathogen Coxiella burnetii.
    Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5455-60 PMID: 12704232
  22. RelE toxins from bacteria and Archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA.
    Mol Microbiol. 2003 Jun;48(5):1389-400 PMID: 12787364
  23. Bacteriophage P1 Ban protein is a hexameric DNA helicase that interacts with and substitutes for Escherichia coli DnaB.
    Nucleic Acids Res. 2003 Jul 15;31(14):3918-28 PMID: 12853607
  24. Toxin-antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA.
    J Mol Biol. 2003 Sep 26;332(4):809-19 PMID: 12972253
  25. New insights into the formation of active nonsense-mediated decay complexes.
    Trends Biochem Sci. 2003 Sep;28(9):464-6 PMID: 13678954
  26. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli.
    Mol Cell. 2003 Oct;12(4):913-23 PMID: 14580342
  27. New connections in the prokaryotic toxin-antitoxin network: relationship with the eukaryotic nonsense-mediated RNA decay system.
    Genome Biol. 2003;4(12):R81 PMID: 14659018
  28. The YefM antitoxin defines a family of natively unfolded proteins: implications as a novel antibacterial target.
    J Biol Chem. 2004 Feb 27;279(9):8252-61 PMID: 14672926
  29. Shuffling of Sulfolobus genomes by autonomous and non-autonomous mobile elements.
    Biochem Soc Trans. 2004 Apr;32(Pt 2):179-83 PMID: 15046567
  30. Ribosome rescue by tmRNA requires truncated mRNAs.
    J Mol Biol. 2004 Apr 16;338(1):33-41 PMID: 15050821
  31. Distant structural homology leads to the functional characterization of an archaeal PIN domain as an exonuclease.
    J Biol Chem. 2004 Apr 16;279(16):16471-8 PMID: 14734548
  32. Stationary-phase physiology.
    Annu Rev Microbiol. 2004;58:161-81 PMID: 15487934
  33. Mini-F plasmid genes that couple host cell division to plasmid proliferation.
    Proc Natl Acad Sci U S A. 1983 Aug;80(15):4784-8 PMID: 6308648
  34. Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells.
    Proc Natl Acad Sci U S A. 1986 May;83(10):3116-20 PMID: 3517851
  35. 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. 1987 Nov;210(1):101-10 PMID: 3323833
  36. Site-specific insertion of genes into integrons: role of the 59-base element and determination of the recombination cross-over point.
    Mol Microbiol. 1991 Aug;5(8):1941-59 PMID: 1662753
  37. 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. 1992 May 5;225(1):39-52 PMID: 1316444
  38. A Salmonella dublin virulence plasmid locus that affects bacterial growth under nutrient-limited conditions.
    Mol Microbiol. 1992 Jun;6(12):1631-43 PMID: 1495391
  39. Cell killing by the F plasmid CcdB protein involves poisoning of DNA-topoisomerase II complexes.
    J Mol Biol. 1992 Aug 5;226(3):735-45 PMID: 1324324
  40. Definition of a minimal plasmid stabilization system from the broad-host-range plasmid RK2.
    J Bacteriol. 1992 Dec;174(24):8119-32 PMID: 1459960
  41. 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. 1993 Oct 5;233(3):414-28 PMID: 8411153
  42. chpA and chpB, Escherichia coli chromosomal homologs of the pem locus responsible for stable maintenance of plasmid R100.
    J Bacteriol. 1993 Nov;175(21):6850-6 PMID: 8226627
  43. Selfish behavior of restriction-modification systems.
    Science. 1995 Feb 10;267(5199):897-9 PMID: 7846533
  44. DNA restriction-modification systems mediate plasmid maintenance.
    J Bacteriol. 1995 Jun;177(12):3451-4 PMID: 7768854
  45. Translational coupling and limited degradation of a polycistronic messenger modulate differential gene expression in the parD stability system of plasmid R1.
    Mol Gen Genet. 1995 Sep 20;248(5):599-609 PMID: 7476860
  46. Restriction-modification systems as genomic parasites in competition for specific sequences.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):11095-9 PMID: 7479944
  47. Programmed cell death in bacteria: proteic plasmid stabilization systems.
    Mol Microbiol. 1995 Jul;17(2):205-10 PMID: 7494469
  48. Comparison of ccd of F, parDE of RP4, and parD of R1 using a novel conditional replication control system of plasmid R1.
    Mol Microbiol. 1995 Jul;17(2):211-20 PMID: 7494470
  49. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA.
    Science. 1996 Feb 16;271(5251):990-3 PMID: 8584937
  50. A new plasmid-encoded proteic killer gene system: cloning, sequencing, and analyzing hig locus of plasmid Rts1.
    Biochem Biophys Res Commun. 1996 Mar 18;220(2):280-4 PMID: 8645296
  51. An Escherichia coli chromosomal "addiction module" regulated by guanosine [corrected] 3',5'-bispyrophosphate: a model for programmed bacterial cell death.
    Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):6059-63 PMID: 8650219
  52. A distinctive class of integron in the Vibrio cholerae genome.
    Science. 1998 Apr 24;280(5363):605-8 PMID: 9554855
  53. The Escherichia coli relBE genes belong to a new toxin-antitoxin gene family.
    Mol Microbiol. 1998 Aug;29(4):1065-76 PMID: 9767574
  54. The genome sequence of Rickettsia prowazekii and the origin of mitochondria.
    Nature. 1998 Nov 12;396(6707):133-40 PMID: 9823893
  55. Toxin-antitoxin modules may regulate synthesis of macromolecules during nutritional stress.
    J Bacteriol. 2000 Feb;182(3):561-72 PMID: 10633087
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2005-00-00
Epub
2005-00-17
Pages
966-76
Language
English
Region
England
NLM ID
0411011
PMCID
PMC549392
Subset
IM
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