Escherichia coli resistance to nonbiocidal antibiofilm polysaccharides is rare and mediated by multiple mutations leading to surface physicochemical modifications

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 8, 2013, Pages 3960-3968

  Travier, Laetitia ^a,b   Rendueles, Olaya ^a,b   Ferrières, Lionel ^a,b   Herry, Jean Marie ^c   Ghigo, Jean Marc ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c UMR1319 MICALIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSULE POLYSACCHARIDE; LEWIS BASE; POLYMYXIN B; POLYSACCHARIDE; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENETICS; BACTERIAL MUTATION; BACTERIAL STRAIN; BIOFILM; ESCHERICHIA COLI; GENE EXPRESSION; HYDROPHOBICITY; MINIMUM INHIBITORY CONCENTRATION; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; TRANSPOSON;

ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; BIOFILMS; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; GENES, BACTERIAL; LEWIS BASES; MICROBIAL SENSITIVITY TESTS; MUTATION; PHYSICOCHEMICAL PROCESSES; POLYMYXIN B; POLYSACCHARIDES; POLYSORBATES;

EID: 84880296807     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02606-12     Document Type: Article

References (60)

1. Barczak AK, Hung DT. 2009. Productive steps toward an antimicrobial targeting virulence. Curr. Opin. Microbiol. 12:490-496.
2. Martinez JL, Fajardo A, Garmendia L, Hernandez A, Linares JF, Martínez-Solano L, Sánchez MB. 2009. A global view of antibiotic resistance. FEMS Microbiol. Rev. 33:44-65.
3. Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. 2010. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35:322-332.
4. Lewis K. 2008. Multidrug tolerance of biofilms and persister cells. Curr. Top. Microbiol. Immunol. 322:107-131.
5. Danese PN. 2002. Antibiofilm approaches: prevention of catheter colonization. Chem. Biol. 9:873-880.
6. Vasilev K, Cook J, Griesser HJ. 2009. Antibacterial surfaces for biomedical devices. Expert Rev. Med. Devices 6:553-567.
7. Martins MCL, Costa F, Carvalho IF, Montelaro RC, Gomes P. 2010. Covalent immobilization of antimicrobial peptides (AMPs) onto biomaterial surfaces. Acta Biomater. 7:1431-1440.
8. Rasko DA, Sperandio V. 2010. Anti-virulence strategies to combat bacteria-mediated disease. Nat. Rev. Drug Discov. 9:117-128.
9. Rendueles O, Ghigo JM. 24 January 2012. Multi-species biofilms: how to avoid unfriendly neighbors. FEMS Microbiol. Rev. [Epub ahead of print.] doi:10.1111/j.1574-6976.2012.00328.x.
10. Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Høiby N, Kjelleberg S, Givskov M. 2002. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology (Reading, Engl.) 148:87-102.
11. Antoniani D, Bocci P, Maciag A, Raffaelli N, Landini P. 2010. Monitoring of diguanylate cyclase activity and of cyclic-di-GMP biosynthesis by whole-cell assays suitable for high-throughput screening of biofilm inhibitors. Appl. Microbiol. Biotechnol. 85:1095-1104.
12. Eguchi Y, Kubo N, Matsunaga H, Igarashi M, Utsumi R. 2011. Development of an antivirulence drug against Streptococcus mutans: repression of biofilm formation, acid tolerance, and competence by a histidine kinase inhibitor, walkmycin C. Antimicrob. Agents Chemother. 55:1475-1484.
13. Pinkner JS, Remaut H, Buelens F, Miller E, Aberg V, Pemberton N, Hedenström M, Larsson A, Seed P, Waksman G, Hultgren SJ, Almqvist F. 2006. Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. Proc. Natl. Acad. Sci. U. S. A. 103:17897-17902.
14. Banat IM, Franzetti A, Gandolfi I, Bestetti G, Martinotti MG, Fracchia L, Smyth TJ, Marchant R. 2010. Microbial biosurfactants production, applications and future potential. Appl. Microbiol. Biotechnol. 87:427-444.
15. Ron EZ, Rosenberg E. 2001. Natural roles of biosurfactants. Environ. Microbiol. 3:229-236.
16. Boles B, Thoendel M, Singh P. 2005. Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol. Microbiol. 57:1210-1223.
17. Rivardo F, Turner RJ, Allegrone G, Ceri H, Martinotti MG. 2009. Anti-adhesion activity of two biosurfactants produced by Bacillus spp. prevents biofilm formation of human bacterial pathogens. Appl. Microbiol. Biotechnol. 83:541-553.
18. Kiran GS, Sabarathnam B, Selvin J. 2010. Biofilm disruption potential of a glycolipid biosurfactant from marine Brevibacterium casei. FEMS Immunol. Med. Microbiol. 59:432-438.
19. Valle J, Da Re S, Henry N, Fontaine T, Balestrino D, Latour-Lambert P, Ghigo JM. 2006. Broad-spectrum biofilm inhibition by a secreted bacterial polysaccharide. Proc. Natl. Acad. Sci. U. S. A. 103:12558-12563.
20. Da Re S, Le Quere 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.
21. Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F. 1951. A colorimetric method for the determination of sugars. Nature 168:167.
22. Hacek DM, Dressel DC, Peterson LR. 1999. Highly reproducible bactericidal activity test results by using a modified National Committee for Clinical Laboratory Standards broth macrodilution technique. J. Clin. Microbiol. 37:1881-1884.
23. Ferrières L, Hémery G, Nham T, Guérout A-M, Mazel D, Beloin C, Ghigo J-M. 2010. Silent mischief: bacteriophage Mu insertions contaminate products of Escherichia coli random mutagenesis performed using suicidal transposon delivery plasmids mobilized by broad-host-range RP4 conjugative machinery. J. Bacteriol. 192:6418-6427.
24. Da Re S, Ghigo J-M. 2006. A CsgD-independent pathway for cellulose production and biofilm formation in Escherichia coli. J. Bacteriol. 188: 3073-3087.
25. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio Collection. Mol. Syst. Biol. 2:2006.0008.
26. Chaveroche MK, Ghigo JM, d'Enfert C. 2000. A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res. 28:E97. doi:10.1093/nar/28.22.e97.
27. Lesic B, Bach S, Ghigo JM, Dobrindt U, Hacker J, Carniel E. 2004. Excision of the high-pathogenicity island of Yersinia pseudotuberculosis requires the combined actions of its cognate integrase and Hef, a new recombination directionality factor. Mol. Microbiol. 52:1337-1348.
28. Cherepanov PP, Wackernagel W. 1995. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14.
29. Briandet R, Herry J, Bellon-Fontaine M. 2001. Determination of the van der Waals, electron donor and electron acceptor surface tension components of static Gram-positive microbial biofilms. Colloids Surf. B 21:299-310.
30. Bernier SP, Lebeux D, DeFrancesco AS, Valomon A, Soubigou G, Coppée JY, Ghigo JM, Beloin C. 2012. Starvation together with the SOS response mediates high biofilm-specific tolerance to the fluoroquinolone ofloxacin. PLoS Genet. 9:e1003144. doi:10.1371/journal.pgen.1003144.
31. Ghigo JM. 2001. Natural conjugative plasmids induce bacterial biofilm development. Nature 412:442-445.
32. Palmer J, Flint S, Brooks J. 2007. Bacterial cell attachment, the beginning of a biofilm. J. Ind. Microbiol. Biotechnol. 34:577-588.
33. Eginton PJ, Holah J, Allison DG, Handley PS, Gilbert P. 1998. Changes in the strength of attachment of micro-organisms to surfaces following treatment with disinfectants and cleansing agents. Lett. Appl. Microbiol. 27:101-105.
34. Mireles JR, II, Toguchi A, Harshey RM. 2001. Salmonella enterica serovar Typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation. J. Bacteriol. 183:5848-5854.
35. Rendueles O, Travier L, Latour-Lambert P, Fontaine T, Magnus J, Denamur E, Ghigo J-M. 2011. Screening of Escherichia coli species biodiversity reveals new biofilm-associated antiadhesion polysaccharides. mBio 2(3):e00043-11. doi:10.1128/mBio.00043-11.
36. Cegelski L, Marshall GR, Eldridge GR, Hultgren SJ. 2008. The biology and future prospects of antivirulence therapies. Nat. Rev. Microbiol. 6:17-27.
37. Kohler T, Perron GG, Buckling A, van Delden C. 2010. Quorum sensing inhibition selects for virulence and cooperation in Pseudomonas aeruginosa. PLoS Pathog. 6:e1000883. doi:10.1371/journal.ppat.1000883.
38. Maeda T, Garcia-Contreras R, Pu M, Sheng L, Garcia LR, Tomas M, Wood TK. 2012. Quorum quenching quandary: resistance to antivirulence compounds. ISME J. 6:493-501.
39. Kraus D, Peschel A. 2006. Molecular mechanisms of bacterial resistance to antimicrobial peptides. Curr. Top. Microbiol. Immunol. 306:231-250.
40. Meehl M, Herbert S, Gotz F, Cheung A. 2007. Interaction of the GraRS two-component system with the VraFG ABC transporter to support vancomycin-intermediate resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 51:2679-2689.
41. Hankins JV, Madsen JA, Giles DK, Brodbelt JS, Trent MS. 2012. Amino acid addition to Vibrio cholerae LPS establishes a link between surface remodeling in Gram-positive and Gram-negative bacteria. Proc. Natl. Acad. Sci. U. S. A. 109:8722-8727.
42. Ribeiro RM, Bonhoeffer S. 2000. Production of resistant HIV mutants during antiretroviral therapy. Proc. Natl. Acad. Sci. U. S. A. 97:7681-7686.
43. Komarova NL, Wodarz D. 2005. Drug resistance in cancer: principles of emergence and prevention. Proc. Natl. Acad. Sci. U. S. A. 102:9714-9719.
44. Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, Agata T, Mizunoe Y. 2010. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465:346-349.
45. Mellbye B, Schuster M. 2011. The sociomicrobiology of antivirulence drug resistance: a proof of concept. mBio 2(5):e00131-11. doi:10.1128/mBio.00131-11.
46. Paul M, Leibovici L. 2009. Combination antimicrobial treatment versus monotherapy: the contribution of meta-analyses. Infect. Dis. Clin. North Am. 23:277-293.
47. Mitchell G, Lafrance M, Boulanger S, Seguin DL, Guay I, Gattuso M, Marsault E, Bouarab K, Malouin F. 2012. Tomatidine acts in synergy with aminoglycoside antibiotics against multiresistant Staphylococcus aureus and prevents virulence gene expression. J. Antimicrob. Chemother. 67:559-568.
48. Chauhan A, Lebeaux D, Decante B, Kriegel I, Escande MC, Ghigo JM, Beloin C. 2012. A rat model of central venous catheter to study establishment of long-term bacterial biofilm and related acute and chronic infections. PLoS One 7:e37281. doi:10.1371/journal.pone.0037281.
49. Pao S, Paulsen I, Saier M, Jr. 1998. Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 62:1.
50. Vaknin A, Berg H. 2008. Direct evidence for coupling between bacterial chemoreceptors. J. Mol. Biol. 382:573-577.
51. Postma PW, Lengeler JW, Jacobson GR. 1993. Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57: 543-594.
52. Chao KL, Lim K, Lehmann C, Doseeva V, Howard AJ, Schwarz FP, Herzberg O. 2008. The Escherichia coli YdcF binds S-adenosyl-Lmethionine and adopts an alpha/beta-fold characteristic of nucleotideutilizing enzymes. Proteins 72:506-509.
53. Molloy M, Herbert B, Slade M, Rabilloud T, Nouwens A, Williams K, Gooley A. 2000. Proteomic analysis of the Escherichia coli outer membrane. Eur. J. Biochem. 267:2871-2881.
54. Horazdovsky BF, Hogg RW. 1989. Genetic reconstitution of the highaffinity L-arabinose transport system. J. Bacteriol. 171:3053-3059.
55. Sawers G, Bock A. 1989. Novel transcriptional control of the pyruvate formate-lyase gene: upstream regulatory sequences and multiple promoters regulate anaerobic expression. J. Bacteriol. 171:2485-2498.
56. Basturea GN, Rudd KE, Deutscher MP. 2006. Identification and characterization of RsmE, the founding member of a new RNA base methyltransferase family. RNA 12:426-434.
57. Yakovleva G, Kim S, Wanner B. 1998. Phosphate-independent expression of the carbon-phosphorus lyase activity of Escherichia coli. Appl. Microbiol. Biotechnol. 49:573-578.
58. Nagakubo S, Nishino K, Hirata T, Yamaguchi A. 2002. The putative response regulator BaeR stimulates multidrug resistance of Escherichia coli via a novel multidrug exporter system, MdtABC. J. Bacteriol. 184: 4161-4167.
59. Voloshin ON, Vanevski F, Khil PP, Camerini-Otero RD. 2003. Characterization of the DNA damage-inducible helicase DinG from Escherichia coli. J. Biol. Chem. 278:28284-28293.
60. Kim KS, Pelton JG, Inwood WB, Andersen U, Kustu S, Wemmer DE. 2010. The Rut pathway for pyrimidine degradation: novel chemistry and toxicity problems. J. Bacteriol. 192:4089-4102.