Unmasking the ancestral activity of integron integrases reveals a smooth evolutionary transition during functional innovation

Nature Communications

Volumn 7, Issue , 2016, Pages

  Escudero, Jose Antonio ^a,b   Loot, Celine ^a,b   Parissi, Vincent ^c   Nivina, Aleksandra ^a,b,d   Bouchier, Christiane ^a   Mazel, Didier ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c University Victor Segalen   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HOST FACTOR; INTEGRASE; BACTERIAL PROTEIN; CRUCIFORM DNA; DNA; ESCHERICHIA COLI PROTEIN; SINGLE STRANDED DNA;

ANCESTRY; ASYMMETRY; DNA; EVOLUTIONARY BIOLOGY; HYBRID; PERSISTENCE; RECOMBINATION;

ANTIBIOTIC RESISTANCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; INTEGRON; MOLECULAR EVOLUTION; NONHUMAN; REPLICON; COMPUTER SIMULATION; CONFORMATION; ENTEROBACTERIA PHAGE LAMBDA; GENETICS; IN VITRO STUDY; METABOLISM; PROTEIN TERTIARY STRUCTURE; VIBRIO CHOLERAE;

BACTERIAL PROTEINS; BACTERIOPHAGE LAMBDA; COMPUTER SIMULATION; DNA; DNA, CRUCIFORM; DNA, SINGLE-STRANDED; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EVOLUTION, MOLECULAR; IN VITRO TECHNIQUES; INTEGRASES; INTEGRONS; NUCLEIC ACID CONFORMATION; PROTEIN STRUCTURE, TERTIARY; VIBRIO CHOLERAE;

EID: 84960851447     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10937     Document Type: Article

References (60)

1. Grindley, N. D., Whiteson, K. L. & Rice, P. A. Mechanisms of site-specific recombination. Annu. Rev. Biochem. 75, 567-605 (2006).
2. Landy, A. The lambda integrase site-specific recombination pathway. Microbiol Spectr 3, MDNA3-0051-2014 (2015).
3. Golden, J. W., Robinson, S. J. & Haselkorn, R. Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena. Nature 314, 419-423 (1985).
4. Val, M. E., Skovgaard, O., Ducos-Galand, M., Bland, M. J. & Mazel, D. Genome engineering in Vibrio cholerae: a feasible approach to address biological issues. PLoS Genet. 8, e1002472 (2012).
5. Sherratt, D. J. & Wigley, D. B. Conserved themes but novel activities in recombinases and topoisomerases. Cell 93, 149-152 (1998).
6. Toth-Petroczy, A. & Tawfik, D. S. The robustness and innovability of protein folds. Curr. Opin. Struct. Biol. 26, 131-138 (2014).
7. Kobryn, K. & Chaconas, G. Hairpin Telomere Resolvases. Microbiol. Spectr. 2, MDNA3-0023-2014 (2014).
8. Mazel, D. Integrons: agents of bacterial evolution. Nat. Rev. Microbiol. 4, 608-620 (2006).
9. Recchia, G. D. & Hall, R. M. Gene cassettes: a new class of mobile element. Microbiology 141, 3015-3027 (1995).
10. Escudero, J. A., Loot, C., Nivina, A. & Mazel, D. The Integron: Adaptation On Demand. Microbiol. Spectr. 3, MDNA3-0019-2014 (2015).
11. Rowe-Magnus, D. A. et al. The evolutionary history of chromosomal super-integrons provides an ancestry for multiresistant integrons. Proc. Natl Acad. Sci. USA 98, 652-657 (2001).
12. Rowe-Magnus, D. A. & Mazel, D. The role of integrons in antibiotic resistance gene capture. Int. J. Med. Microbiol. 292, 115-125 (2002).
13. Martinez, E. & de la Cruz, F. Genetic elements involved in Tn21 site-specific integration, a novel mechanism for the dissemination of antibiotic resistance genes. EMBO J. 9, 1275-1281 (1990).
14. Hall, R. M., Brookes, D. E. & Stokes, H. W. Site-specific insertion of genes into integrons-role of the 59-base element and determination of the recombination cross-over point. Mol. Microbiol. 5, 1941-1959 (1991).
15. Frumerie, C., Ducos-Galand, M., Gopaul, D. N. & Mazel, D. The relaxed requirements of the integron cleavage site allow predictable changes in integron target specificity. Nucleic Acids Res. 38, 559-569 (2010).
16. Francia, M. V., Zabala, J. C., de la Cruz, F. & Garcia-Lobo, J. M. The IntI1 integron integrase preferentially binds single-stranded DNA of the attC site. J. Bacteriol. 181, 6844-6849 (1999).
17. Bouvier, M., Demarre, G. & Mazel, D. Integron cassette insertion: a recombination process involving a folded single strand substrate. EMBO J. 24, 4356-4367 (2005).
18. Cambray, G., Guerout, A. M. & Mazel, D. Integrons. Annu. Rev. Genet. 44, 141-166 (2010).
19. Bouvier, M., Ducos-Galand, M., Loot, C., Bikard, D. & Mazel, D. Structural features of single-stranded integron cassette attC sites and their role in strand selection. PLoS Genet. 5, e1000632 (2009).
20. MacDonald, D., Demarre, G., Bouvier, M., Mazel, D. & Gopaul, D. N. Structural basis for broad DNA-specificity in integron recombination. Nature 440, 1157-1162 (2006).
21. Loot, C., Ducos-Galand, M., Escudero, J. A., Bouvier, M. & Mazel, D. Replicative resolution of integron cassette insertion. Nucleic Acids Res. 40, 8361-8370 (2012).
22. Nunes-Duby, S. E., Kwon, H. J., Tirumalai, R. S., Ellenberger, T. & Landy, A. Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res. 26, 391-406 (1998).
23. Toll-Riera, M. & Alba, M. M. Emergence of novel domains in proteins. BMC Evol. Biol. 13, 47 (2013).
24. Aroul-Selvam, R., Hubbard, T. & Sasidharan, R. Domain insertions in protein structures. J. Mol. Biol. 338, 633-641 (2004).
25. Guerin, E. et al. The SOS response controls integron recombination. Science 324, 1034 (2009).
26. Wagner, A. The molecular origins of evolutionary innovations. Trends Genet. 27, 397-410 (2011).
27. Demarre, G., Frumerie, C., Gopaul, D. N. & Mazel, D. Identification of key structural determinants of the IntI1 integron integrase that influence attC x attI1 recombination efficiency. Nucleic Acids Res. 35, 6475-6489 (2007).
28. Loot, C. et al. The integron integrase efficiently prevents the melting effect of Escherichia coli single-stranded DNA-binding protein on folded attC sites. J. Bacteriol. 196, 762-771 (2014).
29. Collis, C. M., Kim, M. J., Stokes, H. W. & Hall, R. M. Integron-encoded IntI integrases preferentially recognize the adjacent cognate attI site in recombination with a 59-be site. Mol. Microbiol. 46, 1415-1427 (2002).
30. Partridge, S. R. et al. Definition of the attI1 site of class 1 integrons. Microbiology 146, 2855-2864 (2000).
31. Tokuriki, N. & Tawfik, D. S. Protein dynamism and evolvability. Science 324, 203-207 (2009).
32. Lloyd, R. G. & Sharples, G. J. Dissociation of synthetic Holliday junctions by E. coli RecG protein. EMBO J. 12, 17-22 (1993).
33. Tsaneva, I. R., Muller, B. & West, S. C. ATP-dependent branch migration of Holliday junctions promoted by the RuvA and RuvB proteins of E. coli. Cell 69, 1171-1180 (1992).
34. Connolly, B. et al. Resolution of Holliday junctions in vitro requires the Escherichia coli ruvC gene product. Proc. Natl Acad. Sci. USA 88, 6063-6067 (1991).
35. Biskri, L., Bouvier, M., Guerout, A. M., Boisnard, S. & Mazel, D. Comparative study of class 1 Integron and Vibrio cholerae superintegron integrase activities. J. Bacteriol. 187, 1740-1750 (2005).
36. Baharoglu, Z., Bikard, D. & Mazel, D. Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLoS Genet. 6, e1001165 (2010).
37. Hansson, K., Skold, O. & Sundstrom, L. Non-palindromic attl sites of integrons are capable of site-specific recombination with one another and with secondary targets. Mol. Microbiol. 26, 441-453 (1997).
38. Gravel, A., Fournier, B. & Roy, P. H. DNA complexes obtained with the integron integrase IntI1 at the attI1 site. Nucleic Acids Res. 26, 4347-4355 (1998).
39. Messier, N. & Roy, P. H. Integron integrases possess a unique additional domain necessary for activity. J. Bacteriol. 183, 6699-6706 (2001).
40. Dubois, V., Debreyer, C., Litvak, S., Quentin, C. & Parissi, V. A new in vitro strand transfer assay for monitoring bacterial class 1 integron recombinase IntI1 activity. PLoS ONE 2, e1315 (2007).
41. Gonzalez-Zorn, B. et al. Genetic basis for dissemination of armA. J. Antimicrob. Chemother. 56, 583-585 (2005).
42. Boyd, D., Cloeckaert, A., Chaslus-Dancla, E. & Mulvey, M. R. Characterization of variant Salmonella genomic island 1 multidrug resistance regions from serovars Typhimurium DT104 and Agona. Antimicrob. Agents Chemother. 46, 1714-1722 (2002).
43. Hamidian, M., Holt, K. E. & Hall, R. M. Genomic resistance island AGI1 carrying a complex class 1 integron in a multiply antibiotic-resistant ST25 Acinetobacter baumannii isolate. J. Antimicrob. Chemother. 70, 2519-2523 (2015).
44. Baharoglu, Z., Krin, E. & Mazel, D. Connecting environment and genome plasticity in the characterization of transformation-induced SOS regulation and carbon catabolite control of the Vibrio cholerae integron integrase. J. Bacteriol. 194, 1659-1667 (2012).
45. Chandler, M. et al. Breaking and joining single-stranded DNA: the HUH endonuclease superfamily. Nat. Rev. Microbiol. 11, 525-538 (2013).
46. San Millan, A. et al. Sequencing of plasmids pAMBL1 and pAMBL2 from Pseudomonas aeruginosa reveals a blaVIM-1 amplification causing high-level carbapenem resistance. J. Antimicrob. Chemother. 70, 3000-3003 (2015).
47. Val, M. E. et al. The single-stranded genome of phage CTX is the form used for integration into the genome of Vibrio cholerae. Mol. Cell 19, 559-566 (2005).
48. Quinones, M., Kimsey, H. H. & Waldor, M. K. LexA cleavage is required for CTX prophage induction. Mol. Cell 17, 291-300 (2005).
49. Das, B., Martinez, E., Midonet, C. & Barre, F. X. Integrative mobile elements exploiting Xer recombination. Trends Microbiol. 21, 23-30 (2013).
50. Midonet, C. & Barre, F. X. Xer site-specific recombination: promoting vertical and horizontal transmission of genetic information. Microbiol. Spectr. 2, MDNA3-0056-2014 (2014).
51. Waldor, M. K. & Mekalanos, J. J. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910-1914 (1996).
52. Campbell, A., del-Campillo-Campbell, A. & Ginsberg, M. L. Specificity in DNA recognition by phage integrases. Gene 300, 13-18 (2002).
53. Gottfried, P., Yagil, E. & Kolot, M. Core-binding specificity of bacteriophage integrases. Mol. Gen. Genet. 263, 619-624 (2000).
54. Yagil, E., Dorgai, L. & Weisberg, R. A. Identifying determinants of recombination specificity: construction and characterization of chimeric bacteriophage integrases. J. Mol. Biol. 252, 163-177 (1995).
55. Tawfik, D. S. Accuracy-rate tradeoffs: how do enzymes meet demands of selectivity and catalytic efficiency? Curr. Opin. Chem. Biol. 21, 73-80 (2014).
56. Demarre, G. et al. A new family of mobilizable suicide plasmids based on the broad host range R388 plasmid (IncW) or RP4 plasmid (IncPa) conjugative machineries and their cognate E.coli host strains. Res. Microbiol. 156, 245-255 (2005).
57. Sambrook, J., Fritsch, E. F. & Maniatis, T. Molecular Cloning: A Laboratory Manual (Cold Spring Harbour Laboratory Press, 1989).
58. Loot, C., Bikard, D., Rachlin, A. & Mazel, D. Cellular pathways controlling integron cassette site folding. EMBO J. 29, 2623-2634 (2010).
59. Dubois, V., Debreyer, C., Quentin, C. & Parissi, V. In vitro recombination catalyzed by bacterial class 1 integron integrase IntI1 involves cooperative binding and specific oligomeric intermediates. PLoS ONE 4, e5228 (2009).
60. Martin, S. S., Chu, V. C. & Baldwin, E. Modulation of the active complex assembly and turnover rate by protein-DNA interactions in Cre-LoxP recombination. Biochemistry 42, 6814-6826 (2003).