The stringent response promotes antibiotic resistance dissemination by regulating integron integrase expression in biofilms

mBio

Volumn 7, Issue 4, 2016, Pages

  Strugeon, Emilie ^a,b   Tilloy, Valentin ^a   Ploy, Marie Cécile ^a   Da Re, Sandra ^a  

^a UNIVERSITY OF LIMOGES   (France)

^b Euromedex   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CLASS 1 INTEGRON INTEGRASE; ENDOPEPTIDASE LA; INTEGRASE; PINTI1 PROTEIN; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BIOFILM; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; GENE CASSETTE; GENE EXPRESSION; GRAM NEGATIVE BACTERIUM; INTEGRON; INTI1 GENE; LEXA GENE; NONHUMAN; PRIORITY JOURNAL; REGULON; REPRESSOR GENE; SFIA GENE; BIOSYNTHESIS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; SOS RESPONSE (GENETICS);

BIOFILMS; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION REGULATION, BACTERIAL; INTEGRASES; INTEGRONS; PROTEASE LA; SOS RESPONSE (GENETICS);

EID: 84986626356     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00868-16     Document Type: Article

References (70)

1. Davies, J, Davies D. 2010. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74:417–433. http://dx.doi.org/10.1128/MMBR.00016-10.
2. Kalan, L, Wright GD. 2011. Antibiotic adjuvants: multicomponent antiinfective strategies. Expert Rev Mol Med 13:e5. http://dx.doi.org/10.1017/S1462399410001766.
3. Cambray, G, Guerout AM, Mazel D. 2010. Integrons. Annu Rev Genet 44:141–166. http://dx.doi.org/10.1146/annurev-genet-102209-163504.
4. Gillings, MR. 2014. Integrons: past, present, and future. Microbiol Mol Biol Rev 78:257–277. http://dx.doi.org/10.1128/MMBR.00056-13.
5. Stokes, HW, Hall RM. 1989. A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: integrons. Mol Microbiol 3:1669–1683. http://dx.doi.org/10.1111/j.1365-2958.1989.tb00153.x.
6. Collis, CM, Hall RM. 1992. Site-specific deletion and rearrangement of integron insert genes catalyzed by the integron DNA integrase. J Bacteriol 174:1574–1585.
7. Mazel, D. 2006. Integrons: agents of bacterial evolution. Nat Rev Microbiol 4:608–620. http://dx.doi.org/10.1038/nrmicro1462.
8. Boucher, Y, Labbate M, Koenig JE, Stokes HW. 2007. Integrons: mobilizable platforms that promote genetic diversity in bacteria. Trends Microbiol 15:301–309. http://dx.doi.org/10.1016/j.tim.2007.05.004.
9. Cury, J, Jové T, Touchon M, Néron B, Rocha EP. 2016. Identification and analysis of integrons and cassette arrays in bacterial genomes. Nucleic Acids Res 44:4539–4550. http://dx.doi.org/10.1093/nar/gkw319.
10. Domingues, S, da Silva GJ, Nielsen KM. 2012. Integrons: vehicles and pathways for horizontal dissemination in bacteria. Mob Genet Elements 2:211–223. http://dx.doi.org/10.4161/mge.22967.
11. Partridge, SR, Tsafnat G, Coiera E, Iredell JR. 2009. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 33: 757–784. http://dx.doi.org/10.1111/j.1574-6976.2009.00175.x.
12. Guerin, E, Cambray G, Sanchez-Alberola N, Campoy S, Erill I, Da Re S, Gonzalez-Zorn B, Barbé J, Ploy MC, Mazel D. 2009. The, SOS response controls integron recombination. Science 324:1034. http://dx.doi.org/10.1126/science.1172914.
13. Erill, I, Campoy S, Barbé J. 2007. Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol Rev 31: 637–656. http://dx.doi.org/10.1111/j.1574-6976.2007.00082.x.
14. Walker, GC. 1984. Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol Res 48:60–93.
15. Courcelle, J, Khodursky A, Peter B, Brown PO, Hanawalt PC. 2001. Comparative gene expression profiles followingUVexposure in wild-type and SOS-deficient Escherichia coli. Genetics 158:41–64.
16. Fernández D, De Henestrosa AR, Ogi T, Aoyagi S, Chafin D, Hayes JJ, Ohmori H, Woodgate R. 2000. Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol Microbiol 35:1560–1572. http://dx.doi.org/10.1046/j.1365-2958.2000.01826.x.
17. Little, JW. 1991. Mechanism of specific LexA cleavage: autodigestion and the role of RecA coprotease. Biochimie 73:411–421. http://dx.doi.org/10.1016/0300-9084(91)90108-D.
18. Baharoglu, Z, Bikard D, Mazel D. 2010. Conjugative, DNA transfer induces the bacterial SOS response and promotes antibiotic resistance de- velopment through integron activation. PLoS Genet 6:e1001165. http://dx.doi.org/10.1371/journal.pgen.1001165.
19. Baharoglu, Z, Krin E, Mazel D. 2012. 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. http://dx.doi.org/10.1128/JB.05982-11.
20. Baharoglu, Z, Mazel D. 2011. Vibrio cholerae triggers SOS and mutagenesis in response to a wide range of antibiotics: a route towards multiresistance. Antimicrob Agents Chemother 55:2438–2441. http://dx.doi.org/10.1128/AAC.01549-10.
21. Cagle, CA, Shearer JE, Summers AO. 2011. Regulation of the integrase and cassette promoters of the class 1 integron by nucleoid-associated proteins. Microbiology 157:2841–2853. http://dx.doi.org/10.1099/mic.0.046987-0.
22. Monds, RD, O’Toole GA. 2009. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol 17: 73–87. http://dx.doi.org/10.1016/j.tim.2008.11.001.
23. Stewart, PS, Costerton JW. 2001. Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138. http://dx.doi.org/10.1016/S0140-6736(01)05321-1.
24. Lebeaux, D, Ghigo JM, Beloin C. 2014. Biofilm-related infections: bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics. Microbiol Mol Biol Rev 78:510–543. http://dx.doi.org/10.1128/MMBR.00013-14.
25. Van, Acker H, Van Dijck P, Coenye T. 2014. Molecular mechanisms of antimicrobial tolerance and resistance in bacterial and fungal biofilms. Trends Microbiol 22:326–333. http://dx.doi.org/10.1016/j.tim.2014.02.001.
26. Lewis, K. 2010. Persister cells. Annu Rev Microbiol 64:357–372. http://dx.doi.org/10.1146/annurev.micro.112408.134306.
27. Shah, D, Zhang Z, Khodursky A, Kaldalu N, Kurg K, Lewis K. 2006. Persisters: a distinct physiological state of E. coli. BMC Microbiol 6:53. http://dx.doi.org/10.1186/1471-2180-6-53.
28. Bernier, SP, Lebeaux D, DeFrancesco AS, Valomon A, Soubigou G, Coppée JY, Ghigo JM, Beloin C. 2013. Starvation, together with the SOS response, mediates high biofilm-specific tolerance to the fluoroquinolone ofloxacin. PLoS Genet 9:e1003144. http://dx.doi.org/10.1371/journal.pgen.1003144.
29. Boles, BR, Singh PK. 2008. Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc Natl Acad Sci U S A 105:12503–12508. http://dx.doi.org/10.1073/pnas.0801499105.
30. Stewart, PS, Franklin MJ. 2008. Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210. http://dx.doi.org/10.1038/nrmicro1838.
31. Maeda, S, Ito M, Ando T, Ishimoto Y, Fujisawa Y, Takahashi H, Matsuda A, Sawamura A, Kato S. 2006. Horizontal transfer of nonconjugative plasmids in a colony biofilm of Escherichia coli. FEMS Microbiol Lett 255:115–120. http://dx.doi.org/10.1111/j.1574-6968.2005.00072.x.
32. Molin, S, Tolker-Nielsen T. 2003. Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 14:255–261. http://dx.doi.org/10.1016/S0958-1669(03)00036-3.
33. Hennequin, C, Aumeran C, Robin F, Traore O, Forestier C. 2012. Antibiotic resistance and plasmid transfer capacity in biofilm formed with a CTX-M-15-producing Klebsiella pneumoniae isolate. J Antimicrob Chemother 67:2123–2130. http://dx.doi.org/10.1093/jac/dks169.
34. Madsen, JS, Burmølle M, Hansen LH, Sørensen SJ. 2012. The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunol Med Microbiol 65:183–195. http://dx.doi.org/10.1111/j.1574-695X.2012.00960.x.
35. Gaze, WH, Zhang L, Abdouslam NA, Hawkey PM, Calvo-Bado L, Royle J, Brown H, Davis S, Kay P, Boxall AB, Wellington EM. 2011. Impacts of anthropogenic activity on the ecology of class 1 integrons and integronassociated genes in the environment. ISME J 5:1253–1261. http://dx.doi.org/10.1038/ismej.2011.15.
36. Stalder, T, Barraud O, Casellas M, Dagot C, Ploy MC. 2012. Integron involvement in environmental spread of antibiotic resistance. Front Microbiol 3:119. http://dx.doi.org/10.3389/fmicb.2012.00119.
37. Stalder, T, Barraud O, Jové T, Casellas M, Gaschet M, Dagot C, Ploy MC. 2014. Quantitative and qualitative impact of hospital effluent on dissemination of the integron pool. ISME J 8:768–777. http://dx.doi.org/10.1038/ismej.2013.189.
38. Ghigo, JM. 2001. Natural conjugative plasmids induce bacterial biofilm development. Nature 412:442–445. http://dx.doi.org/10.1038/35086581.
39. Lutz, R, Bujard H. 1997. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res 25:1203–1210. http://dx.doi.org/10.1093/nar/25.6.1203.
40. Görke, B, Stülke J. 2008. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6:613–624. http://dx.doi.org/10.1038/nrmicro1932.
41. Rojo, F. 2010. Carbon catabolite repression in Pseudomonas: optimizing metabolic versatility and interactions with the environment. FEMS Microbiol Rev 34:658–684. http://dx.doi.org/10.1111/j.1574-6976.2010.00218.x.
42. Ploy, MC, Courvalin P, Lambert T. 1998. Characterization of In40 of Enterobacter aerogenes BM2688, a class 1 integron with two new gene cassettes, cmlA2 and qacF. Antimicrob Agents Chemother 42:2557–2563.
43. Kalia, D, Merey G, Nakayama S, Zheng Y, Zhou J, Luo Y, Guo M, Roembke BT, Sintim HO. 2013. Nucleotide, c-di-GMP, c-di-AMP, cGMP, cAMP, (p)ppGpp signaling in bacteria and implications in pathogenesis. Chem Soc Rev 42:305–341. http://dx.doi.org/10.1039/c2cs35206k.
44. Landini, P. 2009. Cross-talk mechanisms in biofilm formation and responses to environmental and physiological stress in Escherichia coli. Res Microbiol 160:259–266. http://dx.doi.org/10.1016/j.resmic.2009.03.001.
45. Dalebroux, ZD, Swanson MS. 2012. ppGpp: magic beyond RNA polymerase. Nat Rev Microbiol 10:203–212. http://dx.doi.org/10.1038/nrmicro2720.
46. Potrykus, K, Cashel M. 2008. (p)ppGpp: still magical? Annu Rev Microbiol 62: 35203–51. http://dx.doi.org/10.1146/annurev.micro.62.081307.162903.
47. Srivatsan, A, Wang JD. 2008. Control of bacterial transcription, translation and replication by (p)ppGpp. Curr Opin Microbiol 11:100–105. http://dx.doi.org/10.1016/j.mib.2008.02.001.
48. Kingston, RE, Nierman WC, Chamberlin MJ. 1981. A direct effect of guanosine tetraphosphate on pausing of Escherichia coli RNA polymerase during RNA chain elongation. J Biol Chem 256:2787–2797.
49. Krohn, M, Wagner R. 1996. Transcriptional pausing of RNA polymerase in the presence of guanosine tetraphosphate depends on the promoter and gene sequence. J Biol Chem 271:23884–23894. http://dx.doi.org/10.1074/jbc.271.39.23884.
50. McGlynn P, Savery NJ, Dillingham MS. 2012. The conflict between DNA replication and transcription. Mol Microbiol 85:12–20. http://dx.doi.org/10.1111/j.1365-2958.2012.08102.x.
51. Gan, W, Guan Z, Liu J, Gui T, Shen K, Manley JL, Li X. 2011. R-loopmediated genomic instability is caused by impairment of replication fork progression. Genes Dev 25:2041–2056. http://dx.doi.org/10.1101/gad.17010011.
52. Durfee, T, Hansen AM, Zhi H, Blattner FR, Jin DJ. 2008. Transcription profiling of the stringent response in Escherichia coli. J Bacteriol 190: 1084–1096. http://dx.doi.org/10.1128/JB.01092-07.
53. Gaca, AO, Colomer-Winter C, Lemos JA. 2015. Many means to a common end: the intricacies of (p)ppGpp metabolism and its control of bacterial homeostasis. J Bacteriol 197:1146–1156. http://dx.doi.org/10.1128/JB.02577-14.
54. Hauryliuk, V, Atkinson GC, Murakami KS, Tenson T, Gerdes K. 2015. Recent functional insights into the role of (p)ppGpp in bacterial physiology. Nat Rev Microbiol 13:298–309. http://dx.doi.org/10.1038/nrmicro3448.
55. Kuroda, A. 2006. A polyphosphate-lon protease complex in the adaptation of Escherichia coli to amino acid starvation. Biosci Biotechnol Biochem 70:325–331. http://dx.doi.org/10.1271/bbb.70.325.
56. Tsilibaris, V, Maenhaut-Michel G, Van Melderen L. 2006. Biological roles of the Lon ATP-dependent protease. Res Microbiol 157:701–713. http://dx.doi.org/10.1016/j.resmic.2006.05.004.
57. Nomura, K, Kato J, Takiguchi N, Ohtake H, Kuroda A. 2004. Effects of inorganic polyphosphate on the proteolytic and DNA-binding activities of Lon in Escherichia coli. J Biol Chem 279:34406–34410. http://dx.doi.org/10.1074/jbc.M404725200.
58. Osbourne, DO, Soo VW, Konieczny I, Wood TK. 2014. Polyphosphate, cyclic AMP, guanosine tetraphosphate, and c-di-GMP reduce in vitro Lon activity. Bioengineered 5:264–268. http://dx.doi.org/10.4161/bioe.29261.
59. Huang, CT, Xu KD, McFeters GA, Stewart PS. 1998. Spatial patterns of alkaline phosphatase expression within bacterial colonies and biofilms in response to phosphate starvation. Appl Environ Microbiol 64:1526–1531.
60. Amato, SM, Brynildsen MP. 2014. Nutrient transitions are a source of persisters in Escherichia coli biofilms. PLoS One 9:e93110. http://dx.doi.org/10.1371/journal.pone.0093110.
61. Amato, SM, Orman MA, Brynildsen MP. 2013. Metabolic control of persister formation in Escherichia coli. Mol Cell 50:475–487. http://dx.doi.org/10.1016/j.molcel.2013.04.002.
62. Maisonneuve, E, Castro-Camargo M, Gerdes K. 2013. (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154:1140–1150. http://dx.doi.org/10.1016/j.cell.2013.07.048.
63. Nguyen, D, Joshi-Datar A, Lepine F, Bauerle E, Olakanmi O, Beer K, McKay G, Siehnel R, Schafhauser J, Wang Y, Britigan BE, Singh PK. 2011. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334:982–986. http://dx.doi.org/10.1126/science.1211037.
64. Gillings, M, Boucher Y, Labbate M, Holmes A, Krishnan S, Holley M, Stokes HW. 2008. The evolution of class 1 integrons and the rise of antibiotic resistance. J Bacteriol 190:5095–5100. http://dx.doi.org/10.1128/JB.00152-08.
65. Koenig, JE, Boucher Y, Charlebois RL, Nesbø C, Zhaxybayeva O, Bapteste E, Spencer M, Joss MJ, Stokes HW, Doolittle WF. 2008. Integronassociated gene cassettes in Halifax Harbour: assessment of a mobile gene pool in marine sediments. Environ Microbiol 10:1024–1038. http://dx.doi.org/10.1111/j.1462-2920.2007.01524.x.
66. Cherepanov, PP, Wackernagel W. 1995. Gene disruption in Escherichia coli: TcR andKmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9–14. http://dx.doi.org/10.1016/0378-1119(95)00193-A.
67. Da, Re S, Le Quéré B, Ghigo JM, Beloin C. 2007. Tight modulation of Escherichia coli bacterial biofilm formation through controlled expression of adhesion factors. Appl Environ Microbiol 73:3391–3403. http://dx.doi.org/10.1128/AEM.02625-06.
68. Jové, T, Da Re S, Denis F, Mazel D, Ploy MC. 2010. Inverse correlation between promoter strength and excision activity in class 1 integrons. PLoS Genet 6:e1000793. http://dx.doi.org/10.1371/journal.pgen.1000793.
69. Espéli, O, Moulin L, Boccard F. 2001. Transcription attenuation associated with bacterial repetitive extragenic BIME elements. J Mol Biol 314: 375–386. http://dx.doi.org/10.1006/jmbi.2001.5150.
70. Beloin, C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, Balestrino D, Haagensen JA, Molin S, Prensier G, Arbeille B, Ghigo JM. 2004. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51:659–674. http://dx.doi.org/10.1046/j.1365-2958.2003.03865.x.