Exploring the HME and HAE1 efflux systems in the genus Burkholderia

BMC Evolutionary Biology

Volumn 10, Issue 1, 2010, Pages

  Perrin, Elena ^a   Fondi, Marco ^a   Papaleo, Maria Cristiana ^a   Maida, Isabel ^a   Buroni, Silvia ^b   Pasca, Maria Rosalia ^b   Riccardi, Giovanna ^b   Fani, Renato ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC RESISTANCE; BACTERIUM; BIOCHEMISTRY; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENOME; HEALTH RISK; PATHOGEN; PHYLOGENETICS; PROTEIN; PUBLIC HEALTH; SUBSTRATE;

BACTERIA (MICROORGANISMS); BURKHOLDERIA;

OUTER MEMBRANE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BURKHOLDERIA; CONSENSUS SEQUENCE; GENE; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIDRUG RESISTANCE; PHYLOGENY; PROTEIN MOTIF; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; BURKHOLDERIA; CONSENSUS SEQUENCE; DRUG RESISTANCE, MULTIPLE, BACTERIAL; EVOLUTION, MOLECULAR; GENES, BACTERIAL; GENES, MDR; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN;

EID: 77953013067     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-10-164     Document Type: Article

References (78)

1. Diversity and occurrence of Burkholderia spp. in the natural environment. S Compant J Nowak T Coenye C Clement E Ait Barka, FEMS Microbiol Rev 2008 32 4 607 626 10.1111/j.1574-6976.2008.00113.x 18422616
2. Diversity and significance of Burkholderia species occupying diverse ecological niches. T Coenye P Vandamme, Environ Microbiol 2003 5 9 719 729 10.1046/j.1462-2920.2003.00471.x 12919407
3. Burkholderia latens sp. nov., Burkholderia diffusa sp. nov., Burkholderia arboris sp. nov., Burkholderia seminalis sp. nov. and Burkholderia metallica sp. nov., novel species within the Burkholderia cepacia complex. E Vanlaere JJ Lipuma A Baldwin D Henry E De Brandt E Mahenthiralingam D Speert C Dowson P Vandamme, Int J Syst Evol Microbiol 2008 58 Pt 7 1580 1590 10.1099/ijs.0.65634-0 18599699
4. Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. E Vanlaere A Baldwin D Gevers D Henry E De Brandt JJ LiPuma E Mahenthiralingam DP Speert C Dowson P Vandamme, Int J Syst Evol Microbiol 2009 59 Pt 1 102 111 10.1099/ijs.0.001123-0 19126732
5. Evolving epidemiology of Pseudomonas aeruginosa and the Burkholderia cepacia complex in cystic fibrosis lung infection. JR Govan AR Brown AM Jones, Future Microbiol 2007 2 153 164 10.2217/17460913.2.2.153 17661652
6. Preventing drug access to targets: cell surface permeability barriers and active efflux in bacteria. H Nikaido, Semin Cell Dev Biol 2001 12 3 215 223 10.1006/scdb.2000.0247 11428914
7. Efflux in bacteria: what do we really know about it? BM Ryan TJ Dougherty D Beaulieu J Chuang BA Dougherty JF Barrett, Expert Opin Investig Drugs 2001 10 8 1409 1422 10.1517/13543784.10.8.1409 11772259
8. Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems. JL Martinez MB Sanchez L Martinez-Solano A Hernandez L Garmendia A Fajardo C Alvarez-Ortega, FEMS Microbiol Rev 2009 33 2 430 449 10.1111/j.1574-6976.2008.00157.x 19207745
9. Evolutionary origins of multidrug and drug-specific efflux pumps in bacteria. MH Saier Jr IT Paulsen MK Sliwinski SS Pao RA Skurray H Nikaido, FASEB J 1998 12 3 265 274 9506471
10. Cells need safety valves. A Danchin, Bioessays 2009 31 7 769 773 10.1002/bies.200900024 19472369
11. Proton-dependent multidrug efflux systems. IT Paulsen MH Brown RA Skurray, Microbiol Rev 1996 60 4 575 608 8987357
12. Efflux pumps as antimicrobial resistance mechanisms. K Poole, Ann Med 2007 39 3 162 176 10.1080/07853890701195262 17457715
13. Phylogeny of multidrug transporters. MH Saier Jr IT Paulsen, Semin Cell Dev Biol 2001 12 3 205 213 10.1006/scdb.2000.0246 11428913
14. Genetic locus encoding functions involved in biosynthesis and outer membrane localization of xanthomonadin in Xanthomonas oryzae pv. oryzae. AK Goel L Rajagopal N Nagesh RV Sonti, J Bacteriol 2002 184 13 3539 3548 10.1128/JB.184.13.3539-3548.2002 12057948
15. Multiple antibiotic resistance in Pseudomonas aeruginosa: evidence for involvement of an efflux operon. K Poole K Krebes C McNally S Neshat, J Bacteriol 1993 175 22 7363 7372 8226684
16. Molecular cloning and characterization of acrA and acrE genes of Escherichia coli. D Ma DN Cook M Alberti NG Pon H Nikaido JE Hearst, J Bacteriol 1993 175 19 6299 6313 8407802
17. Involvement of an active efflux system in the natural resistance of Pseudomonas aeruginosa to aminoglycosides. JR Aires T Kohler H Nikaido P Plesiat, Antimicrob Agents Chemother 1999 43 11 2624 2628 10543738 (Pubitemid 29519539)
18. Origin and evolution of metabolic pathways. R Fani M Fondi, Physics of Life Reviews 2009 6 23 52 10.1016/j.plrev.2008.12.003
19. Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. MH Saier Jr R Tam A Reizer J Reizer, Mol Microbiol 1994 11 5 841 847 10.1111/j.1365-2958.1994.tb00362.x 8022262
20. Crystal structure of bacterial multidrug efflux transporter AcrB. S Murakami R Nakashima E Yamashita A Yamaguchi, Nature 2002 419 6907 587 593 10.1038/nature01050 12374972
21. Structure of the periplasmic component of a bacterial drug efflux pump. MK Higgins E Bokma E Koronakis C Hughes V Koronakis, Proc Natl Acad Sci USA 2004 101 27 9994 9999 10.1073/pnas.0400375101 15226509
22. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. V Koronakis A Sharff E Koronakis B Luisi C Hughes, Nature 2000 405 6789 914 919 10.1038/35016007 10879525
23. Crystal structure of the drug discharge outer membrane protein, OprM, of Pseudomonas aeruginosa: dual modes of membrane anchoring and occluded cavity end. H Akama M Kanemaki M Yoshimura T Tsukihara T Kashiwagi H Yoneyama S Narita A Nakagawa T Nakae, J Biol Chem 2004 279 51 52816 52819 10.1074/jbc.C400445200 15507433
24. Crystal structure of the membrane fusion protein, MexA, of the multidrug transporter in Pseudomonas aeruginosa. H Akama T Matsuura S Kashiwagi H Yoneyama S Narita T Tsukihara A Nakagawa T Nakae, J Biol Chem 2004 279 25 25939 25942 10.1074/jbc.C400164200 15117957
25. Crystal structure of the multidrug exporter MexB from Pseudomonas aeruginosa. G Sennhauser MA Bukowska C Briand MG Grutter, J Mol Biol 2009 389 1 134 145 10.1016/j.jmb.2009.04.001 19361527
26. Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. S Murakami R Nakashima E Yamashita T Matsumoto A Yamaguchi, Nature 2006 443 7108 173 179 10.1038/nature05076 16915237
27. Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism. MA Seeger A Schiefner T Eicher F Verrey K Diederichs KM Pos, Science 2006 313 5791 1295 1298 10.1126/science.1131542 16946072
28. The multifarious, multireplicon Burkholderia cepacia complex. E Mahenthiralingam TA Urban JB Goldberg, Nat Rev Microbiol 2005 3 2 144 156 10.1038/nrmicro1085 15643431 (Pubitemid 40207595)
29. The antimicrobial susceptibility of Pseudomonas pseudomallei. Emergence of resistance in vitro and during treatment. DA Dance V Wuthiekanun W Chaowagul NJ White, J Antimicrob Chemother 1989 24 3 295 309 10.1093/jac/24.3.295 2681116
30. Antibiotic susceptibility of 65 isolates of Burkholderia pseudomallei and Burkholderia mallei to 35 antimicrobial agents. FM Thibault E Hernandez DR Vidal M Girardet JD Cavallo, J Antimicrob Chemother 2004 54 6 1134 1138 10.1093/jac/dkh471 15509614
31. Efflux pump genes of the resistance-nodulation-division family in Burkholderia cenocepacia genome. P Guglierame MR Pasca E De Rossi S Buroni P Arrigo G Manina G Riccardi, BMC Microbiol 2006 6 66 10.1186/1471-2180-6-66 16857052
32. The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. MT Holden HM Seth-Smith LC Crossman M Sebaihia SD Bentley AM Cerdeno-Tarraga NR Thomson N Bason MA Quail S Sharp,, et al. J Bacteriol 2009 191 1 261 277 10.1128/JB.01230-08 18931103
33. Nucleotide sequence analysis of a gene from Burkholderia (Pseudomonas) cepacia encoding an outer membrane lipoprotein involved in multiple antibiotic resistance. JL Burns CD Wadsworth JJ Barry CP Goodall, Antimicrob Agents Chemother 1996 40 2 307 313 8834871
34. Salicylate induces an antibiotic efflux pump in Burkholderia cepacia complex genomovar III (B. cenocepacia). BM Nair KJ Cheung Jr A Griffith JL Burns, J Clin Invest 2004 113 3 464 473 14755343
35. Expression of resistance-nodulation-cell-division efflux pumps in commonly used Burkholderia pseudomallei strains and clinical isolates from northern Australia. A Kumar M Mayo LA Trunck AC Cheng BJ Currie HP Schweizer, Trans R Soc Trop Med Hyg 2008 102 Suppl 1 145 151 10.1016/S0035-9203(08)70032-4 19121677
36. Efflux-mediated aminoglycoside and macrolide resistance in Burkholderia pseudomallei. RA Moore D DeShazer S Reckseidler A Weissman DE Woods, Antimicrob Agents Chemother 1999 43 3 465 470 10049252
37. BpeAB-OprB, a multidrug efflux pump in Burkholderia pseudomallei. YY Chan TM Tan YM Ong KL Chua, Antimicrob Agents Chemother 2004 48 4 1128 1135 10.1128/AAC.48.4.1128-1135.2004 15047512
38. Method for regulated expression of single-copy efflux pump genes in a surrogate Pseudomonas aeruginosa strain: identification of the BpeEF-OprC chloramphenicol and trimethoprim efflux pump of Burkholderia pseudomallei 1026b. A Kumar KL Chua HP Schweizer, Antimicrob Agents Chemother 2006 50 10 3460 3463 10.1128/AAC.00440-06 17005832
39. The Burkholderia pseudomallei BpeAB-OprB efflux pump: expression and impact on quorum sensing and virulence. YY Chan KL Chua, J Bacteriol 2005 187 14 4707 4719 10.1128/JB.187.14.4707-4719.2005 15995185
40. Control of quorum sensing by a Burkholderia pseudomallei multidrug efflux pump. YY Chan HS Bian TM Tan ME Mattmann GD Geske J Igarashi T Hatano H Suga HE Blackwell KL Chua, J Bacteriol 2007 189 11 4320 4324 10.1128/JB.00003-07 17384185
41. Comparative genomic analyses of seventeen Streptococcus pneumoniae strains: insights into the pneumococcal supragenome. NL Hiller B Janto JS Hogg R Boissy S Yu E Powell R Keefe NE Ehrlich K Shen J Hayes,, et al. J Bacteriol 2007 189 22 8186 8195 10.1128/JB.00690-07 17675389
42. Integrative conjugative elements and related elements are major contributors to the genome diversity of Streptococcus agalactiae. M Brochet E Couve P Glaser G Guedon S Payot, J Bacteriol 2008 190 20 6913 6917 10.1128/JB.00824-08 18708498
43. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. M Touchon C Hoede O Tenaillon V Barbe S Baeriswyl P Bidet E Bingen S Bonacorsi C Bouchier O Bouvet,, et al. PLoS Genet 2009 5 1 1000344 10.1371/journal.pgen.1000344 19165319
44. Molecular properties of bacterial multidrug transporters. M Putman HW van Veen WN Konings, Microbiol Mol Biol Rev 2000 64 4 672 693 10.1128/MMBR.64.4. 672-693.2000 11104814
45. A simple method for displaying the hydropathic character of a protein. J Kyte RF Doolittle, J Mol Biol 1982 157 1 105 132 10.1016/0022-2836(82)90515-0 7108955
46. Protein Identification and Analysis Tools on the ExPASy Server. E Gasteiger C Hoogland A Gattiker S Duvaud MR Wilkins RD Appel A Bairoch, The Proteomics Protocols Handbook, Humana Press, John M Walker, 2005 571 607
47. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. JD Thompson DG Higgins TJ Gibson, Nucleic Acids Res 1994 22 22 4673 4680 10.1093/nar/22.22.4673 7984417
48. The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. TT Tseng KS Gratwick J Kollman D Park DH Nies A Goffeau MH Saier Jr, J Mol Microbiol Biotechnol 1999 1 1 107 125 10941792
49. Function of the MexB efflux-transporter divided into two halves. S Eda H Yoneyama T Nakae, Biochemistry 2003 42 23 7238 7244 10.1021/bi0300074 12795620
50. Substrate specificity of the RND-type multidrug efflux pumps AcrB and AcrD of Escherichia coli is determined predominantly by two large periplasmic loops. CA Elkins H Nikaido, J Bacteriol 2002 184 23 6490 6498 10.1128/JB.184.23.6490-6499.2002 12426336
51. Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. S Franke G Grass C Rensing DH Nies, J Bacteriol 2003 185 13 3804 3812 10.1128/JB.185.13.3804-3812.2003 12813074
52. On the mechanism of substrate specificity by resistance nodulation division (RND)-type multidrug resistance pumps: the large periplasmic loops of MexD from Pseudomonas aeruginosa are involved in substrate recognition. W Mao MS Warren DS Black T Satou T Murata T Nishino N Gotoh O Lomovskaya, Mol Microbiol 2002 46 3 889 901 10.1046/j.1365-2958.2002.03223.x 12410844
53. Differential impact of MexB mutations on substrate selectivity of the MexAB-OprM multidrug efflux pump of Pseudomonas aeruginosa. JK Middlemiss K Poole, J Bacteriol 2004 186 5 1258 1269 10.1128/JB.186.5.1258-1269.2004 14973037
54. Chimeric analysis of the multicomponent multidrug efflux transporters from gram-negative bacteria. EB Tikhonova Q Wang HI Zgurskaya, J Bacteriol 2002 184 23 6499 6507 10.1128/JB.184.23.6499-6507.2002 12426337
55. Energetics and topology of CzcA, a cation/proton antiporter of the resistance-nodulation-cell division protein family. M Goldberg T Pribyl S Juhnke DH Nies, J Biol Chem 1999 274 37 26065 26070 10.1074/jbc.274.37.26065 10473554
56. Identification of essential charged residues in transmembrane segments of the multidrug transporter MexB of Pseudomonas aeruginosa. L Guan T Nakae, J Bacteriol 2001 183 5 1734 1739 10.1128/JB.183.5.1734-1739.2001 11160105
57. TCDB: the Transporter Classification Database for membrane transport protein analyses and information. MH Saier Jr CV Tran RD Barabote, Nucleic Acids Res 2006 34 Database issue 181 186 10.1093/nar/gkj001 16381841
58. Threonine-978 in the transmembrane segment of the multidrug efflux pump AcrB of Escherichia coli is crucial for drug transport as a probable component of the proton relay network. Y Takatsuka H Nikaido, J Bacteriol 2006 188 20 7284 7289 10.1128/JB.00683-06 17015667
59. Crystal structure of the multidrug efflux transporter AcrB at 3.1A resolution reveals the N-terminal region with conserved amino acids. D Das QS Xu JY Lee I Ankoudinova C Huang Y Lou A DeGiovanni R Kim SH Kim, J Struct Biol 2007 158 3 494 502 10.1016/j.jsb.2006.12.004 17275331
60. Comparative analyses of fundamental differences in membrane transport capabilities in prokaryotes and eukaryotes. Q Ren IT Paulsen, PLoS Comput Biol 2005 1 3 27 10.1371/journal.pcbi.0010027 16118665
61. Structural, evolutionary and genetic analysis of the histidine biosynthetic "Core" in the genus Burkholderia. MC Papaleo E Russo M Fondi G Emiliani A Frandi M Brilli R Pastorelli R Fani, Gene 2009 448 1 16 28 10.1016/j.gene.2009.08.002 19683039
62. From the primordial soup to the latest universal common ancestor. M Vaneechoutte R Fani, Res Microbiol 2009 160 7 437 440 10.1016/j.resmic.2009.09. 002 19751826
63. Horizontal gene transfer and the earliest stages of the evolution of life. AM Poole, Res Microbiol 2009 160 7 473 480 10.1016/j.resmic.2009.07.009 19647074
64. Contribution of gene loss to the pathogenic evolution of Burkholderia pseudomallei and Burkholderia mallei. RA Moore S Reckseidler-Zenteno H Kim W Nierman Y Yu A Tuanyok J Warawa D DeShazer DE Woods, Infect Immun 2004 72 7 4172 4187 10.1128/IAI.72.7.4172-4187.2004 15213162
65. Enzyme recruitment in evolution of new function. RA Jensen, Annu Rev Microbiol 1976 30 409 425 10.1146/annurev.mi.30.100176.002205 791073
66. Origin and evolution of operons and metabolic pathways. M Fondi G Emiliani R Fani, Res Microbiol 2009 160 7 502 512 10.1016/j.resmic.2009.05.001 19465116
67. Structural basis of multiple drug-binding capacity of the AcrB multidrug efflux pump. EW Yu G McDermott HI Zgurskaya H Nikaido DE Koshland Jr, Science 2003 300 5621 976 980 10.1126/science.1083137 12738864
68. AcrB multidrug efflux pump of Escherichia coli: composite substrate-binding cavity of exceptional flexibility generates its extremely wide substrate specificity. EW Yu JR Aires H Nikaido, J Bacteriol 2003 185 19 5657 5664 10.1128/JB.185.19.5657-5664.2003 13129936
69. A periplasmic drug-binding site of the AcrB multidrug efflux pump: a crystallographic and site-directed mutagenesis study. EW Yu JR Aires G McDermott H Nikaido, J Bacteriol 2005 187 19 6804 6815 10.1128/JB.187.19.6804-6815.2005 16166543
70. Site-directed mutagenesis reveals putative substrate binding residues in the Escherichia coli RND efflux pump AcrB. JA Bohnert S Schuster MA Seeger E Fahnrich KM Pos WV Kern, J Bacteriol 2008 190 24 8225 8229 10.1128/JB.00912-08 18849422
71. Mechanisms of RND multidrug efflux pumps. H Nikaido Y Takatsuka, Biochim Biophys Acta 2009 1794 5 769 781 19026770
72. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman, Nucleic Acids Res 1997 25 17 3389 3402 10.1093/nar/25.17.3389 9254694
73. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. JR Cole Q Wang E Cardenas J Fish B Chai RJ Farris AS Kulam-Syed-Mohideen DM McGarrell T Marsh GM Garrity,, et al. Nucleic Acids Res 2009 37 Database issue 141 145 10.1093/nar/gkn879 19004872
74. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. TA Hall, Nucl Acids Symp Ser 1999 41 95 98
75. MUSCLE: multiple sequence alignment with high accuracy and high throughput. RC Edgar, Nucleic Acids Res 2004 32 5 1792 1797 10.1093/nar/gkh340 15034147
76. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. K Tamura J Dudley M Nei S Kumar, Mol Biol Evol 2007 24 8 1596 1599 10.1093/molbev/msm092 17488738
77. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. S Guindon O Gascuel, Syst Biol 2003 52 5 696 704 10.1080/10635150390235520 14530136
78. WebLogo: a sequence logo generator. GE Crooks G Hon JM Chandonia SE Brenner, Genome Res 2004 14 6 1188 1190 10.1101/gr.849004 15173120