Negative Feedback and Transcriptional Overshooting in a Regulatory Network for Horizontal Gene Transfer

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Horizontal gene transfer (HGT) is a major force driving bacterial evolution. Because of their ability to cross inter-species barriers, bacterial plasmids are essential agents for HGT. This ability, however, poses specific requisites on plasmid physiology, in particular the need to overcome a multilevel selection process with opposing demands. We analyzed the transcriptional network of plasmid R388, one of the most promiscuous plasmids in Proteobacteria. Transcriptional analysis by fluorescence expression profiling and quantitative PCR revealed a regulatory network controlled by six transcriptional repressors. The regulatory network relied on strong promoters, which were tightly repressed in negative feedback loops. Computational simulations and theoretical analysis indicated that this architecture would show a transcriptional burst after plasmid conjugation, linking the magnitude of the feedback gain with the intensity of the transcriptional burst. Experimental analysis showed that transcriptional overshooting occurred when the plasmid invaded a new population of susceptible cells. We propose that transcriptional overshooting allows genome rebooting after horizontal gene transfer, and might have an adaptive role in overcoming the opposing demands of multilevel selection.

Vyšlo v časopise: Negative Feedback and Transcriptional Overshooting in a Regulatory Network for Horizontal Gene Transfer. PLoS Genet 10(2): e32767. doi:10.1371/journal.pgen.1004171
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004171

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Zdroje

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

2. de la CruzF, DaviesJ (2000) Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol 8 : 128–133.

3. Fernandez-LopezR, Garcillan-BarciaMP, RevillaC, LazaroM, VielvaL, et al. (2006) Dynamics of the IncW genetic backbone imply general trends in conjugative plasmid evolution. FEMS Microbiol Rev 30 : 942–966.

4. SenD, BrownCJ, TopEM, SullivanJ (2013) Inferring the Evolutionary History of IncP-1 Plasmids Despite Incongruence among Backbone Gene Trees. Molecular biology and evolution 30 : 154–166.

5. BoumaJE, LenskiRE (1988) Evolution of a bacteria/plasmid association. Nature 335 : 351–352.

6. DionisioF, ConceicaoIC, MarquesAC, FernandesL, GordoI (2005) The evolution of a conjugative plasmid and its ability to increase bacterial fitness. Biol Lett 1 : 250–252.

7. De GelderL, PoncianoJM, JoyceP, TopEM (2007) Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship. Microbiology 153 : 452–463.

8. HaftRJ, MittlerJE, TraxlerB (2009) Competition favours reduced cost of plasmids to host bacteria. ISME J 3(7): 761–9.

9. PaulssonJ (2002) Multileveled selection on plasmid replication. Genetics 161 : 1373–1384.

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

11. BingleLE, ThomasCM (2001) Regulatory circuits for plasmid survival. Curr Opin Microbiol 4 : 194–200.

12. PolzleitnerE, ZechnerEL, RennerW, FratteR, JaukB, et al. (1997) TraM of plasmid R1 controls transfer gene expression as an integrated control element in a complex regulatory network. Mol Microbiol 25 : 495–507.

13. KoraimannG, TeferleK, MarkolinG, WogerW, HogenauerG (1996) The FinOP repressor system of plasmid R1: analysis of the antisense RNA control of traJ expression and conjugative DNA transfer. Mol Microbiol 21 : 811–821.

14. ThomasCM (2006) Transcription regulatory circuits in bacterial plasmids. Biochem Soc Trans 34 : 1072–1074.

15. DunnyGM, JohnsonCM Regulatory circuits controlling enterococcal conjugation: lessons for functional genomics. Curr Opin Microbiol 14 : 174–180.

16. OgerP, KimKS, SackettRL, PiperKR, FarrandSK (1998) Octopine-type Ti plasmids code for a mannopine-inducible dominant-negative allele of traR, the quorum-sensing activator that regulates Ti plasmid conjugal transfer. Mol Microbiol 27 : 277–288.

17. McAnullaC, EdwardsA, Sanchez-ContrerasM, SawersRG, DownieJA (2007) Quorum-sensing-regulated transcriptional initiation of plasmid transfer and replication genes in Rhizobium leguminosarum biovar viciae. Microbiology 153 : 2074–2082.

18. SuzukiH, YanoH, BrownCJ, TopEM (2010) Predicting plasmid promiscuity based on genomic signature. J Bacteriol 192 : 6045–6055.

19. ZaslaverA, BrenA, RonenM, ItzkovitzS, KikoinI, et al. (2006) A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat Methods 3 : 623–628.

20. RevillaC, Garcillan-BarciaMP, Fernandez-LopezR, ThomsonNR, SandersM, et al. (2008) Different pathways to acquiring resistance genes illustrated by the recent evolution of IncW plasmids. Antimicrob Agents Chemother 52 : 1472–1480.

21. PfafflMW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.

22. GuynetC, de la CruzF (2011) Plasmid segregation without partition. Mobile genetic elements 1 : 236–241.

23. GuynetC, CuevasA, MoncalianG, de la CruzF (2011) The stb operon balances the requirements for vegetative stability and conjugative transfer of plasmid R388. PLoS genetics 7: e1002073.

24. del CampoI, RuizR, CuevasA, RevillaC, VielvaL, et al. (2012) Determination of conjugation rates on solid surfaces. Plasmid 67 : 174–182.

25. WaldorMK, FriedmanDI (2005) Phage regulatory circuits and virulence gene expression. Current opinion in microbiology 8 : 459–465.

26. CamasFM, BlazquezJ, PoyatosJF (2006) Autogenous and nonautogenous control of response in a genetic network. Proc Natl Acad Sci U S A 103 : 12718–12723.

27. RosenfeldN, ElowitzMB, AlonU (2002) Negative autoregulation speeds the response times of transcription networks. J Mol Biol 323 : 785–793.

28. SchleifR (1988) DNA binding by proteins. Science 241 : 1182–1187.

29. SarkarRR, MaithreyeR, SinhaS (2011) Design of regulation and dynamics in simple biochemical pathways. Journal of mathematical biology 63 : 283–307.

30. LevinBR, StewartFM (1980) The population biology of bacterial plasmids: a priori conditions for the existence of mobilizable nonconjugative factors. Genetics 94 : 425–443.

31. LundquistPD, LevinBR (1986) Transitory derepression and the maintenance of conjugative plasmids. Genetics 113 : 483–497.

32. StewartFM, LevinBR (1977) The Population Biology of Bacterial Plasmids: A PRIORI Conditions for the Existence of Conjugationally Transmitted Factors. Genetics 87 : 209–228.

33. Shen-OrrSS, MiloR, ManganS, AlonU (2002) Network motifs in the transcriptional regulation network of Escherichia coli. Nat Genet 31 : 64–68.

34. Jagura-BurdzyG, ThomasCM (1992) kfrA gene of broad host range plasmid RK2 encodes a novel DNA-binding protein. J Mol Biol 225 : 651–660.

35. Jagura-BurdzyG, ThomasCM (1995) Purification of KorA protein from broad host range plasmid RK2: definition of a hierarchy of KorA operators. J Mol Biol 253 : 39–50.

36. KostelidouK, JonesAC, ThomasCM (1999) Conserved C-terminal region of global repressor KorA of broad-host-range plasmid RK2 is required for co-operativity between KorA and a second RK2 global regulator, KorB. J Mol Biol 289 : 211–221.

37. AdamczykM, DolowyP, JonczykM, ThomasCM, Jagura-BurdzyG (2006) The kfrA gene is the first in a tricistronic operon required for survival of IncP-1 plasmid R751. Microbiology 152 : 1621–1637.

38. BingleLE, RajasekarKV, MuntahaS, NadellaV, HydeEI, et al. (2008) A single aromatic residue in transcriptional repressor protein KorA is critical for cooperativity with its co-regulator KorB. Mol Microbiol 70 : 1502–1514.

39. PansegrauW, LankaE, BarthPT, FigurskiDH, GuineyDG, et al. (1994) Complete nucleotide sequence of Birmingham IncP alpha plasmids. Compilation and comparative analysis. J Mol Biol 239 : 623–663.

40. JacobF, WollmanEL (1956) [Processes of conjugation and recombination in Escherichia coli. I. Induction by conjugation or zygotic induction]. Annales de l'Institut Pasteur 91 : 486–510.

41. BabicA, LindnerAB, VulicM, StewartEJ, RadmanM (2008) Direct visualization of horizontal gene transfer. Science 319 : 1533–1536.

42. BecskeiA, SerranoL (2000) Engineering stability in gene networks by autoregulation. Nature 405 : 590–593.

43. SavageauMA (1974) Comparison of classical and autogenous systems of regulation in inducible operons. Nature 252 : 546–549.

44. AustinDW, AllenMS, McCollumJM, DarRD, WilgusJR, et al. (2006) Gene network shaping of inherent noise spectra. Nature 439 : 608–611.

45. DasN, Valjavec-GratianM, BasurayAN, FeketeRA, PappPP, et al. (2005) Multiple homeostatic mechanisms in the control of P1 plasmid replication. Proc Natl Acad Sci U S A 102 : 2856–2861.

46. ParkK, HanE, PaulssonJ, ChattorajDK (2001) Origin pairing (‘handcuffing’) as a mode of negative control of P1 plasmid copy number. EMBO J 20 : 7323–7332.

47. Garcillan-BarciaMP, de la CruzF (2008) Why is entry exclusion an essential feature of conjugative plasmids? Plasmid 60 : 1–18.

48. LartigueC, GlassJI, AlperovichN, PieperR, ParmarPP, et al. (2007) Genome transplantation in bacteria: changing one species to another. Science 317 : 632–638.

49. KhlebnikovA, DatsenkoKA, SkaugT, WannerBL, KeaslingJD (2001) Homogeneous expression of the P(BAD) promoter in Escherichia coli by constitutive expression of the low-affinity high-capacity AraE transporter. Microbiology 147 : 3241–3247.

50. BollandS, LlosaM, AvilaP, de la CruzF (1990) General organization of the conjugal transfer genes of the IncW plasmid R388 and interactions between R388 and IncN and IncP plasmids. J Bacteriol 172 : 5795–5802.

51. Fernandez-LopezR, Del CampoI, RuizR, LanzaV, VielvaL, et al. Numbers on the edges: a simplified and scalable method for quantifying the gene regulation function. Bioessays 32 : 346–355.

52. GohEB, YimG, TsuiW, McClureJ, SuretteMG, et al. (2002) Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proceedings of the National Academy of Sciences of the United States of America 99 : 17025–17030.