ArdC, a ssDNA-binding protein with a metalloprotease domain, overpasses the recipient hsdRMS restriction system broadening conjugation host range

English version

Autoři: Lorena González-Montes ^aff001; Irene del Campo ^aff001; M. Pilar Garcillán-Barcia ^aff001; Fernando de la Cruz ^aff001; Gabriel Moncalián ^aff001
Působiště autorů: Departamento de Biología Molecular, Universidad de Cantabria and Instituto de Biomedicina y Biotecnología de Cantabria (IBBTEC), CSIC-Universidad de Cantabria, Santander, Cantabria, Spain ^aff001
Vyšlo v časopise: ArdC, a ssDNA-binding protein with a metalloprotease domain, overpasses the recipient hsdRMS restriction system broadening conjugation host range. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008750
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008750

Souhrn

Plasmids, when transferred by conjugation in natural environments, must overpass restriction-modification systems of the recipient cell. We demonstrate that protein ArdC, encoded by broad host range plasmid R388, was required for conjugation from Escherichia coli to Pseudomonas putida. Expression of ardC was required in the recipient cells, but not in the donor cells. Besides, ardC was not required for conjugation if the hsdRMS system was deleted in P. putida recipient cells. ardC was also required if the hsdRMS system was present in E. coli recipient cells. Thus, ArdC has antirestriction activity against the HsdRMS system and consequently broadens R388 plasmid host range. The crystal structure of ArdC was solved both in the absence and presence of Mn²⁺. ArdC is composed of a non-specific ssDNA binding N-terminal domain and a C-terminal metalloprotease domain, although the metalloprotease activity was not needed for the antirestriction function. We also observed by RNA-seq that ArdC-dependent conjugation triggered an SOS response in the P. putida recipient cells. Our findings give new insights, and open new questions, into the antirestriction strategies developed by plasmids to counteract bacterial restriction strategies and settle into new hosts.

Klíčová slova:

Crystal structure – DNA-binding proteins – Electrophoretic mobility shift assay – Horizontal gene transfer – Metalloproteases – Plasmid construction – Plasmids – Pseudomonas putida

Zdroje

1. Soucy SM, Huang J, Gogarten JP. Horizontal gene transfer: Building the web of life. Nat Rev Genet. 2015;16 : 472–482. doi: 10.1038/nrg3962 26184597

2. Craig MacLean R., San Millan A. The Evolution of Antibiotic Resistance. Science. 2019;365 : 1082–1083. doi: 10.1126/science.aax3879 31515374

3. Garcillán-Barcia MP, de la Cruz F. Why is entry exclusion an essential feature of conjugative plasmids? Plasmid. 2008;60 : 1–18. doi: 10.1016/j.plasmid.2008.03.002 18440635

4. Frost LS, Koraimann G. Regulation of bacterial conjugation: Balancing opportunity with adversity. Future Microbiol. 2010;5 : 1057–1071. doi: 10.2217/fmb.10.70 20632805

5. Petrova V, Chitteni-Pattu S, Drees JC, Inman RB, Cox MM. An SOS Inhibitor that Binds to Free RecA Protein: The PsiB Protein. Mol Cell. 2009;36 : 121–130. doi: 10.1016/j.molcel.2009.07.026 19818715

6. Bagdasarian M, Bailone A, Angulo JF, Scholz P, Bagdasarian M, Devoret R. PsiB, and anti-SOS protein, is transiently expressed by the F sex factor during its transmission to an Escherichia coli K-12 recipient. Mol Microbiol. 1992;6 : 885–893. doi: 10.1111/j.1365-2958.1992.tb01539.x 1318487

7. Marraffini LA. CRISPR-Cas immunity in prokaryotes. Nature. 2015;526 : 55–61. doi: 10.1038/nature15386 26432244

8. Gormley NA, Watson MA, Halford SE. Bacterial Restriction–Modification Systems. Encycl Life Sci. 2005; 1–11. doi: 10.1038/npg.els.0001037

9. Wilkins BM. Plasmid promiscuity: meeting the challenge of DNA immigration control. Environ Microbiol. 2002;4 : 495–500. doi: 10.1046/j.1462-2920.2002.00332.x 12220405

10. Tock MR, Dryden DTF. The biology of restriction and anti-restriction. Curr Opin Microbiol. 2005;8 : 466–472. doi: 10.1016/j.mib.2005.06.003 15979932

11. Murray NE. Type I restriction systems: Sophisticated molecular machines. Microbiol Mol Biol Rev. 2000;64 : 412–434. doi: 10.1128/mmbr.64.2.412-434.2000 10839821

12. Fernández-López R, Pilar Garcillán-Barcia M, Revilla C, Lázaro M, Vielva L, De La Cruz F. Dynamics of the IncW genetic backbone imply general trends in conjugative plasmid evolution. FEMS Microbiol Rev. 2006;30 : 942–966. doi: 10.1111/j.1574-6976.2006.00042.x 17026718

13. Chen CY, Kado CI. Inhibition of Agrobacterium tumefaciens oncogenicity by the osa gene of pSa. J Bacteriol. 1994;176 : 5697–5703. doi: 10.1128/jb.176.18.5697-5703.1994 8083162

14. Belogurov AA, Delver EP, Agafonova O V, Belogurova NG, Lee LY, Kado CI. Antirestriction protein Ard (Type C) encoded by IncW plasmid pSa has a high similarity to the “protein transport” domain of TraC1 primase of promiscuous plasmid RP4. J Mol Biol. 2000;296 : 969–977. doi: 10.1006/jmbi.1999.3493 10686096

15. Krishnan A, Burroughs AM, Iyer LM, Aravind L. Unexpected Evolution of Lesion-Recognition Modules in Eukaryotic NER and Kinetoplast DNA Dynamics Proteins from Bacterial Mobile Elements. iScience. 2018;9 : 192–208. doi: 10.1016/j.isci.2018.10.017 30396152

16. Holm L, Sander C. Dali: a network tool for protein structure comparison. Trends Biochem Sci. 1995;20 : 478–480. doi: 10.1016/s0968-0004(00)89105-7 8578593

17. Min J-H, Pavletich NP. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature. 2007;449 : 570–575. doi: 10.1038/nature06155 17882165

18. Li F, Raczynska JE, Chen Z, Yu H. Structural Insight into DNA-Dependent Activation of Human Metalloprotease Spartan. Cell Rep. 2019;26 : 3336–3346. doi: 10.1016/j.celrep.2019.02.082 30893605

19. Wang Y, Xu Q, Lu H, Lin L, Wang L, Xu H, et al. Protease activity of PprI facilitates DNA damage response: Mn(2+)-dependence and substrate sequence-specificity of the proteolytic reaction. Huen MS-Y, editor. PLoS ONE. 2015;10: e01220 : 1–17. doi: 10.1371/journal.pone.0122071 25811789

20. Cerdà-Costa N, Gomis-Rüth FX. Architecture and function of metallopeptidase catalytic domains. Protein Soc. 2014;23 : 123–144. doi: 10.1002/pro.2400 24596965

21. Fukasawa KM, Hata T, Ono Y, Hirose J. Metal Preferences of Zinc-Binding Motif on Metalloproteases. J Amino Acids. 2011;574816 : 1–7. doi: 10.4061/2011/574816 22312463

22. Matthews BW. Structural Basis of the Action of Thermolysin and Related Zinc Peptidases Inhibitor Binding. Acc Chem Res. 1988;21 : 333–340.

23. Fernandez-Lopez R, del Campo I, Revilla C, Cuevas A, de la Cruz F. Negative Feedback and Transcriptional Overshooting in a Regulatory Network for Horizontal Gene Transfer. PLoS Genet. 2014;10: e10041 : 1–15. doi: 10.1371/journal.pgen.1004171 24586200

24. Merryweather A, Rees CE, Smith NM, Wilkins BM. Role of sog polypeptides specified by plasmid ColIb-P9 and their transfer between conjugating bacteria. EMBO J. 1986;5 : 3007–3012. 3024972

25. Serfiotis-Mitsa D, Herbert AP, Roberts GA, Soares DC, White JH, Blakely GW, et al. The structure of the KlcA and ArdB proteins reveals a novel fold and antirestriction activity against Type I DNA restriction systems in vivo but not in vitro. Nucleic Acids Res. 2010;38 : 1723–1737. doi: 10.1093/nar/gkp1144 20007596

26. Goryanin II, Kudryavtseva AA, Balabanov VP, Biryukova VS, Manukhov IV, Zavilgelsky GB. Antirestriction activities of KlcA (RP4) and ArdB (R64) proteins. FEMS Microbiol Lett. 2018;365. doi: 10.1093/femsle/fny227 30239714

27. Garcillán-Barcia MP, Redondo-Salvo S, Vielva L, de la Cruz F. MOBscan: Automated Annotation of MOB Relaxases. Methods Mol Biol Clifton NJ. 2020;2075 : 295–308. doi: 10.1007/978-1-4939-9877-7_21 31584171

28. Melkina OE, Goryanin II, Zavilgelsky GB. The DNA–mimic antirestriction proteins ArdA ColIB-P9, Arn T4, and Ocr T7 as activators of H-NS-dependent gene transcription. Microbiol Res. 2016;192 : 283–291. doi: 10.1016/j.micres.2016.07.008 27664747

29. Serfiotis-Mitsa D, Herbert AP, Roberts GA, Soares DC, White JH, Blakely GW, et al. The structure of the KlcA and ArdB proteins reveals a novel fold and antirestriction activity against type I DNA restriction systems in vivo but not in vitro. Nucleic Acids Res. 2009;38 : 1723–1737. doi: 10.1093/nar/gkp1144 20007596

30. Devigne A, Ithurbide S, Bouthier de la Tour C, Passot F, Mathieu M, Sommer S, et al. DdrO is an essential protein that regulates the radiation desiccation response and the apoptotic-like cell death in the radioresistant Deinococcus radiodurans bacterium. Mol Microbiol. 2015;96 : 1069–1084. doi: 10.1111/mmi.12991 25754115

31. Baharoglu Z, Bikard D, Mazel D. Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLoS Genet. 2010;6: e100116 : 1–10. doi: 10.1371/journal.pgen.1001165 20975940

32. Roer L, Aarestrup FM, Hasman H. The EcoKI type I restriction-modification system in Escherichia coli affects but is not an absolute barrier for conjugation. J Bacteriol. 2015;197 : 337–342. doi: 10.1128/JB.02418-14 25384481

33. Grant SG, Jessee J, Bloom FR, Hanahan D. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci. 1990;87 : 4645–4649. doi: 10.1073/pnas.87.12.4645 2162051

34. Studier FW, Moffatt BA. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol. 1986;189 : 113–130. doi: 10.1016/0022-2836(86)90385-2 3537305

35. Miroux B, Walker JE. Over-production of proteins in Escherichia coli: Mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol. 1996;260 : 289–298. doi: 10.1006/jmbi.1996.0399 8757792

36. Budisa N, Steipe B, Demange P, Eckerskorn C, Kellermann J, Huber R. High-level biosynthetic substitution of methionine in proteins by its analogs 2-aminohexanoic acid, selenomethionine, telluromethionine and ethionine in Escherichia coli. Eur J Biochem. 1995;230 : 788–796. doi: 10.1111/j.1432-1033.1995.tb20622.x 7607253

37. Yu D, Ellis HM, Lee E-C, Jenkins NA, Copeland NG, Court DL. An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci. 2000;97 : 5978–5983. doi: 10.1073/pnas.100127597 10811905

38. Silver PA, Stirling F, Bitzan L, Way J, Oliver JWK, Redfield E, et al. Rational Design of Evolutionarily Stable Microbial Kill Switches. Mol Cell. 2017;68:.e3 : 686–697. doi: 10.1016/j.molcel.2017.10.033 29149596

39. Lee EC, Yu D, Martinez De Velasco J, Tessarollo L, Swing DA, Court DL, et al. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics. 2001;73 : 56–65. doi: 10.1006/geno.2000.6451 11352566

40. Keasling JD, Wanner BL, Skaug T, Datsenko KA, Khlebnikov A. Homogeneous expression of the PBAD promoter in Escherichia coli by constitutive expression of the low-affinity high-capacity AraE transporter. Microbiology. 2001;147 : 3241–3247. doi: 10.1099/00221287-147-12-3241 11739756

41. del Campo I, Ruiz R, Cuevas A, Revilla C, Vielva L, de la Cruz F. Determination of conjugation rates on solid surfaces. Plasmid. 2012;67 : 174–182. doi: 10.1016/j.plasmid.2012.01.008 22289895

42. Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, et al. The complete genome sequence of Escherichia coli K-12. Science. 1997;277 : 1453–1462. doi: 10.1126/science.277.5331.1453 9278503

43. Wang HH, Isaacs FJ, Carr PA, Sun ZZ, Xu G, Forest CR, et al. Programming cells by multiplex genome engineering and accelerated evolution. Nature. 2009;460 : 894–898. doi: 10.1038/nature08187 19633652

44. Bagdasarian M, Lurz R, Riickert B, Bagdasarian MM, Frey J, Timmis KN. Specific-purpose plasmid cloning vectors II. Broad host range, high copy number, RSF1010-derived gene cloning in Pseudomon. Gene. 1981;16 : 237–247. doi: 10.1016/0378-1119(81)90080-9 6282695

45. Martínez-García E, Nikel PI, Aparicio T, de Lorenzo V. Pseudomonas 2.0: Genetic upgrading of P. putida KT2440 as an enhanced host for heterologous gene expression. Microb Cell Factories. 2014;13 : 1–15. doi: 10.1186/s12934-014-0159-3 25384394

46. Rosenberg C, Huguet T. The pAtC58 plasmid of Agrobacterium tumefaciens is not essential for tumour induction. MGG Mol Gen Genet. 1984;196 : 533–536. doi: 10.1007/BF00436205

47. Datta Naomi & Hedges R. W. Trimethoprim Resistance Conferred by W Plasmids in Enterobacteriaceae. J Gen Microbiol. 1972;72 : 349–355. doi: 10.1099/00221287-72-2-349 4562309

48. Martinez E, de la Cruz F. Transposon Tn21 encodes a RecA-independent site-specific integration system. Mol Gen Genet. 1988;211 : 320–325. doi: 10.1007/bf00330610 2832705

49. Zaslaver A, Bren A, Ronen M, Itzkovitz S, Kikoin I, Shavit S, et al. A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat Methods. 2006;3 : 623–628. doi: 10.1038/nmeth895 16862137

50. West SEH, Schweizer HP, Dall C, Sample AK, Runyen-Janecky LJ. Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa. Gene. 1994;148 : 81–86. doi: 10.1016/0378-1119(94)90237-2 7926843

51. Qiu D, Damron FH, Mima T, Schweizer HP, Yu HD. PBAD-based shuttle vectors for functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria. Appl Environ Microbiol. 2008;74 : 7422–6. doi: 10.1128/AEM.01369-08 18849445

52. Andrews S. FASTQC A Quality Control tool for High Throughput Sequence Data. In: Babraham Institute [Internet]. 2015. Available: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/Help/3AnalysisModules/

53. Ben Langmead, Steven S. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2013;9 : 357–359. doi: 10.1038/nmeth.1923.Fast

54. Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA. Artemis: An integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics. 2012;28 : 464–469. doi: 10.1093/bioinformatics/btr703 22199388

55. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4 : 44–57. doi: 10.1038/nprot.2008.211 19131956

56. Battye TGG, Kontogiannis L, Johnson O, Powell HR, Leslie AGW. iMOSFLM: A new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr. 2011;67 : 271–281. doi: 10.1107/S0907444910048675 21460445

57. Evans P, IUCr. Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr. 2006;62 : 72–82. doi: 10.1107/S0907444905036693 16369096

58. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, et al. Overview of the CCP4 suite and current developments. Acta Crystallographica Section D: Biological Crystallography. 2011. pp. 235–242. doi: 10.1107/S0907444910045749 21460441

59. Afonine P.V.; Grosse-Kunstleve R.W; Adams P.D. The Phenix refinement framework. CCP4 Newsletter on protein Crystallography 42, contribution 8. 2005.

60. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004;60 : 2126–2132. doi: 10.1107/S0907444904019158 15572765

61. Eddy SR. A new generation of homology search tools based on probabilistic inference. Genome Inform Int Conf Genome Inform. 2009;23 : 205–211.

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