An Operon of Three Transcriptional Regulators Controls Horizontal Gene Transfer of the Integrative and Conjugative Element ICE in B13

English version České info

Integrative and conjugative elements (ICEs) are a relatively newly recognized class of mobile elements in bacteria, which integrate at one or more positions in a host chromosome, can be excised, circularized, and transfer by conjugation to a new recipient cell. Genome sequencing indicated that ICEs often carry genes with potential adaptive functions for the host. Various ICE-types have been described and ICEclc is a useful model for a wide class of elements found in Beta- and Gammaproteobacteria. Because ICEs normally remain “silent” in the host chromosome and often lack selectable markers, their lifestyle is difficult to study. One of the characteristics of ICEclc is that transfer is initiated in only 3-5% of donor cells in a population during stationary phase. Here, we describe an operon of three regulatory genes, two of which control the transfer initiation of ICEclc. Our findings suggest that the low transfer rate results from the repression of an activator and that this is essential to minimize the deleterious effect of hyper-activation of transfer initiation. While the individual regulatory genes are quite common on ICEs, they rarely occur in this configuration.

Vyšlo v časopise: An Operon of Three Transcriptional Regulators Controls Horizontal Gene Transfer of the Integrative and Conjugative Element ICE in B13. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004441
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004441

Souhrn

Zdroje

1. KooninEV, WolfYI (2008) Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36: 6688–6719.

2. KloesgesT, PopaO, MartinW, DaganT (2011) Networks of gene sharing among 329 proteobacterial genomes reveal differences in lateral gene transfer frequency at different phylogenetic depths. Mol Biol Evol 28: 1057–1074.

3. RankinDJ, RochaEP, BrownSP (2011) What traits are carried on mobile genetic elements, and why? Heredity 106: 1–10.

4. BeikoRG, HarlowTJ, RaganMA (2005) Highways of gene sharing in prokaryotes. Proc Natl Acad Sci U S A 102: 14332–14337.

5. GogartenJP, TownsendJP (2005) Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3: 679–682.

6. FrostLS, LeplaeR, SummersAO, ToussaintA (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3: 722–732.

7. ThomasCM, NielsenKM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3: 711–721.

8. JuhasM, van der MeerJR, GaillardM, HardingRM, HoodDW, et al. (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 33: 376–393.

9. GuglielminiJ, QuintaisL, Garcillan-BarciaMP, de la CruzF, RochaEPC (2011) The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLoS Genet 7: e1002222.

10. WozniakRA, WaldorMK (2010) Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 8: 552–563.

11. BurrusV, WaldorMK (2004) Shaping bacterial genomes with integrative and conjugative elements. Res Microbiol 155: 376–386.

12. BurrusV, PavlovicG, DecarisB, GuédonG (2002) Conjugative transposons: the tip of the iceberg. Mol Microbiol 46: 601–610.

13. DobrindtU, HochhutB, HentschelU, HackerJ (2004) Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2: 414–424.

14. Bellanger X, Payot S, Leblond-Bourget N, Guedon G (2013) Conjugative and mobilizable genomic islands in bacteria: evolution and diversity. FEMS Microbiol Rev. 10.1111/1574-6976.12058 [epub ahead of print].

15. KlockgetherJ, RevaO, LarbigK, TümmlerB (2004) Sequence analysis of the mobile genome island pKLC102 of Pseudomonas aeruginosa C. J Bacteriol. 186: 518–534.

16. KlockgetherJ, WürdemannD, RevaO, WiehlmannL, TümmlerB (2007) Diversity of the abundant pKLC102/PAGI-2 family of genomic islands in Pseudomonas aeruginosa. J Bacteriol 189: 2443–2459.

17. LeeCA, BabicA, GrossmanAD (2010) Autonomous plasmid-like replication of a conjugative transposon. Mol Microbiol 75: 268–279.

18. AuchtungJM, LeeCA, MonsonRE, LehmanAP, GrossmanAD (2005) Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. Proc Natl Acad Sci U S A 102: 12554–12559.

19. BeaberJW, WaldorMK (2004) Identification of operators and promoters that control SXT conjugative transfer. J Bacteriol 186: 5945–5949.

20. BurrusV, WaldorMK (2003) Control of SXT integration and excision. J Bacteriol 185: 5045–5054.

21. SezonovG, HagègeJ, FriedmannA, GuérineauM (1995) Characterization of pra, a gene for replication control in pSAM2, the integrating element of Streptomyces ambofaciens. Mol Microbiol 17: 533–544.

22. SezonovG, DuchêneA-M, FriedmannA, GuérineauM, PernodetJ-L (1998) Replicase, excisionase, and integrase genes of the Streptomyces element pSAM2 constitute an operon positively regulated by the pra gene. J Bacteriol 180: 3056–3061.

23. SezonovG, PossozC, FriedmannA, PernodetJ-L, GuérineauM (2000) KorSA from the Streptomyces integrative element pSAM2 is a central transcriptional repressor: target genes and binding sites. J Bacteriol 182: 1243–1250.

24. RamsayJP, SullivanJT, JambariN, OrtoriCA, HeebS, et al. (2009) A LuxRI-family regulatory system controls excision and transfer of the Mesorhizobium loti strain R7A symbiosis island by activating expression of two conserved hypothetical genes. Mol Microbiol 73: 1141–1155.

25. RamsayJP, MajorAS, KomarovskyVM, SullivanJT, DyRL, et al. (2013) A widely conserved molecular switch controls quorum sensing and symbiosis island transfer in Mesorhizobium loti through expression of a novel antiactivator. Mol Microbiol 87: 1–13.

26. MinoiaM, GaillardM, ReinhardF, StojanovM, SentchiloV, et al. (2008) Stochasticity and bistability in horizontal transfer control of a genomic island in Pseudomonas. Proc Natl Acad Sci U S A 105: 20792–20797.

27. GaillardM, VallaeysT, VorhölterFJ, MinoiaM, WerlenC, et al. (2006) The clc element of Pseudomonas sp. strain B13, a genomic island with various catabolic properties. J Bacteriol 188: 1999–2013.

28. Miyazaki R, Minoia M, Pradervand N, Sentchilo V, Sulser S, et al.. (2011) The clc element and related genomic islands in Proteobacteria. In: Roberts AP, Mullany P, editors. Bacterial integrative mobile genetic elements: Landes Bioscience.

29. MiyazakiR, MinoiaM, PradervandN, SulserS, ReinhardF, et al. (2012) Cellular variability of RpoS expression underlies subpopulation activation of an integrative and conjugative element. PLoS Genet 8: e1002818.

30. ReinhardF, MiyazakiR, PradervandN, van der MeerJR (2013) Cell differentiation to “mating bodies” induced by an integrating and conjugative element in free-living bacteria. Curr Biol 23: 255–259.

31. LarsenRA, WilsonMM, GussAM, MetcalfWW (2002) Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria. Arch Microbiol 178: 193–201.

32. GaillardM, PradervandN, MinoiaM, SentchiloV, JohnsonDR, et al. (2010) Transcriptome analysis of the mobile genome ICEclc in Pseudomonas knackmussii B13. BMC Microbiol 10: 153.

33. MiyazakiR, van der MeerJR (2011) A dual functional origin of transfer in the ICEclc genomic island of Pseudomonas knackmussii B13. Mol Microbiol 79: 743–758.

34. SentchiloVS, RavatnR, WerlenC, ZehnderAJB, van der MeerJR (2003) Unusual integrase gene expression on the clc genomic island of Pseudomonas sp. strain B13. J Bacteriol 185: 4530–4538.

35. LechnerM, SchmittK, BauerS, HotD, HubansC, et al. (2009) Genomic island excisions in Bordetella petrii. BMC Microbiol 9: 141.

36. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.

37. Gerhardt P, Murray RGE, Costilow RN, Nester EW, Wood WA, et al., editors (1981) Manual of methods for general bacteriology. Washington, D.C.: American Society for Microbiology.

38. Martinez-GarciaE, de LorenzoV (2011) Engineering multiple genomic deletions in Gram-negative bacteria: analysis of the multi-resistant antibiotic profile of Pseudomonas putida KT2440. Environ Microbiol 13: 2702–2716.

39. ChoiKH, GaynorJB, WhiteKG, LopezC, BosioCM, et al. (2005) A Tn7-based broad-range bacterial cloning and expression system. Nat Methods 2: 443–448.

40. KochB, JensenLE, NybroeO (2001) A panel of Tn7-based vectors for insertion of the gfp marker gene or for delivery of cloned DNA into Gram-negative bacteria at a neutral chromosomal site. J Microbiol Methods 45: 187–195.

41. Reinhard F, van der Meer JR (2010) Microcolony growth assays In: Timmis KN, de Lorenzo V, McGenity T, van der Meer JR, editors. Handbook of Hydrocarbon and Lipid Microbiology: Springer Verlag. pp. 3562-3570.

42. AbbottJC, AanensenDM, BentleySD (2007) WebACT: an online genome comparison suite. Methods Mol Biol 395: 57–74.

43. DornE, HellwigM, ReinekeW, KnackmussH-J (1974) Isolation and characterization of a 3-chlorobenzoate degrading Pseudomonad. Arch Microbiol 99: 61–70.

44. McClureNC, WeightmanAJ, FryJC (1989) Survival of Pseudomonas putida UWC1 containing cloned catabolic genes in a model activated-sludge unit. Appl Environ Microbiol 55: 2627–2634.

45. SentchiloV, CzechowskaK, PradervandN, MinoiaM, MiyazakiR, et al. (2009) Intracellular excision and reintegration dynamics of the ICEclc genomic island of Pseudomonas knackmussii sp. strain B13. Mol Microbiol 72: 1293–1306.