Table 1.
Resistance-nodulation-division (RND) family multidrug efflux transporters in Gram-negative bacteria and mycobacteria reported or further characterized since 2003
Species | Efflux system componenta |
Regulator (Family) | Substratesb | References | ||
---|---|---|---|---|---|---|
MFP | RND | OMP | ||||
Acinetobacter baumannii | AdeI | AdeJ | AdeK | ? | AO, BL, CM, EM, FQ, FU, LC, NO, PY, RF, SA, SDS, TC, TM | [286, 296] |
Acinetobacter genospecies 3 | AdeD | AdeF | ? | ? | AM, CM, CP, CT, EB, EM, MP, RF, TC | [287, 296] |
AdeX | AdeY | AdeZ | ? | ? | [288, 296] | |
Acinetobacter genospecies UT13 | Unknown | Unknown | AdeC | ? | ? | [733] |
Aeromonas hydrophilia | AheA | AheB | AheC | AheR (TetR) | BC, BL, EM, FU, LC, PR, TC, TM, TT | [223] |
Bacteroides fragilis | BmeA1-16 | BmeB1-16 | BmeC1-16 | Varied, e.g., BmeR5 (TetR) | BL, CP, EB, MD, SDS | [384, 389, 390] |
Brucella suis | BepD | BepE | BepC | BepR (TetR) | AM, BL, CAB, CV, DC, EB, EM, FQ, SDS, TC | [349, 350] |
BepF | BepG | BepC | ? | DC, NA | [350] | |
Burkholderia cenocepacia | CeoA | CeoB | OpcM | CeoR (LysR) | CM, FQ, TMP | [325] |
? | ORF2 | ? | ? | EB, FQ, SM, TPP | [324] | |
Burkholderia glumae | ToxG | ToxH | ToxI | ToxR (LysR) | TF | [610] |
Burkholderia pseudomallei | BpeA | BpeB | OprB | BpeR (TetR) | AC, AG, EM | [326, 327] |
BpeE | BpeF | OprC | BpeT (LysR) | CM, TM | [328] | |
Campylobacter jejuni | CmeD | CmeE | CmeF | ? | AO, AP, CAB, EB, PM, SDS, TR | [371, 373] |
Chromohalobacter spp. | ? | ? | HrdC | ? | BL, CM, EB, OS, TC | [734] |
Enterobacter aerogenes | EefA | EefB | EefC | ? | CM, CP, EM, TC | [182, 735] |
Enterobacter cloacae | AcrA | AcrB | TolC | AcrR (TetR), RamA (MarA) | AC, AG, BL, CL, CM, CP, CV, DC, EM, LC, LZ, SDS, SXT, TC, TG | [736] |
Erwinia amylovora | AcrA | AcrB | ? | AcrR (TetR) | BB, CV, EB, MB, PH, SDS | [596] |
Escherichia coli | OqxA (plasmidborne) | OqxB (plasmidborne) | ? | ORF68 (plasmidborne) | CM, CP, EB, OQ | [154–156] |
Haemophilus influenzae | AcrA | AcrB | ? | AcrR (TetR) | AP | [321, 737] |
Helicobacter pylori | CznB | CznA | CznC | ? | MS | [382] |
HefB | HefC | HefA | ? | CM, CR, CX, EB, GM, ML, NO, TC | [378, 380, 738] | |
Klebsiella pneumoniae | AcrA | AcrB | AcrR | AcrR (TetR), RamA (MarA) | AC, CM, EB, EM, NA, NF, NO, TC, TG | [187, 190, 739] |
EefA | EefB | EefC | ? | Inorganic acid | [191] | |
Morganella morganii | AcrA | AcrB | ? | AcrR (TetR) | AC, CM, EB, EM, NA, NO, SDS, TC, TG, TM | [269] |
Mycobacterium tuberculosis | ? | MmpL7 | ? | ? | INH | [518] |
Neisseria gonorrhoeae | FarA | FarB | MtrE | FarR (MarR) | FA | [740] |
Pasteurella multocida | ? | ? | PM0527 | ? | AO, CT, CV, EB, EM, LC, NO, RF, SDS, TM | [741] |
? | ? | PM1980 | ? | CT, RF, VC. | [741] | |
Proteus mirabilis | AcrA | AcrB | TolC | ? | AC, AP, CM, CP, MI, SAM, SDS, TC, TG, TM | [267] |
Pseudomonas aeruginosa | MexA | MexB | OprM | AmrR, MexR (MarR), NalC (TetR), NalD (TetR) | AC, AO, AG, BL, MC, FQ, NO, OS, SF, TC, TG, TR | [1, 228, 623, 624, 626] |
MexM | MexN | OprM | ? | CM, TP | [264] | |
MexP | MexQ | OpmM | ? | MC, FQ | [264] | |
MexV | MexW | OprM | ? | AC, CM, EB, EM, FQ, TC | [262] | |
TriAB | TriC | OpmH | ? | TR | [123] | |
Pseudomonas fluorescens | EmhA | EmhB | EmhC | ? | Polycyclic aromatic hydrocarbons, CM, NA | [275, 276] |
Pseudomonas stutzeri | TbtA | TbtB | TbtM | ? | CM, NA, OS, SF, TT | [278] |
Pseudomonas syringae | MexA | MexB | OprM | PmeR (TetR) | AC, AG, AO, BB, BC, CM, CV, DA, EB, EM, FQ, FU, NA, NT, RG, TC, TM, TPP | [684] |
PseB | PseC | PseA | GacS/GacA | AC, EM, TC | [590] | |
Ralstonia solanacearum | AcrA | AcrB | ? | AcrR (TetR) | AC, AP, BB, EB | [595] |
Salmonella Typhimurium | MdtA | MdtBC | ? | ? | DC, NO, SDS | [172] |
MsdA | MsdB | MsdC, TolC | ? | DC, NO, SDS | [172] | |
Serratia marcescens | SdeA | SdeB | HasF | SdeR (MarA) | CM, EB, FQ, OS, SDS | [198, 199] |
SdeC | SdeDE | ? | ? | NO | [198, 742] | |
SdeX | SdeY | ? | ? | AC, BAC, EM, NF, RG, TC | [197] | |
Serratia spp. | ZrpAD | ZrpB | ZrpC? | PigZ (TetR) | ? | [206] |
Stenotrophomonas maltophilia | SmeG | SmeH | ? | Smlt3169 (TetR) | ? | [306] |
SmeI | SmeJK | ? | ? | AG, CP, TC | [306] | |
SmeM | SmeN | ? | ? | ? | [306] | |
SmeO | SmeP | ? | Smlt3926 (TetR) | ? | [306] | |
SmeV | SmeW | SmeX | Smlt1827 (LysR) | ? | [306] | |
SmeY | SmeZ | ? | Smlt2199-2130 | AG | [306] | |
Vibrio cholerae | VexA | VexB | ? | VexR (TetR) | MDR | [207–209] |
VexC/BreA | VexD/BreB | ? | VexR/BreR (TetR) | BS | [207–209] | |
VexE | VexF | TolC | ? | BC, BS, DC, EB, EM, NF, NO, SDS, TC, TM | [209] | |
Vibrio parahaemolyticus | VmeA (VP1091) | VmeB (VP1092) | VpoC (VP0425) | ? | AC, BL, CP, CV, DC, EB, EM, NF, RG, SDS, TC, TM | [743] |
MFP=membrane fusion protein; OMP=outer membrane protein; RND=resistance-nodulation-division.
AC=acriflavine; AG=aminoglycosides; AM=amikacin; AO=acridine orange; AP=ampicillin; BC=benzalkonium chloride; BL=β-lactams; BS=bile salts; CAB=cetyltrimethylammonium bromide; CL= cholate; CM=chloramphenicol; CP=ciprofloxacin; CR=clarithromycin; CT=ceftazidime; CV=crystal violet; CX=cefotaxime; DA=daunorubicin, DC=deoxycholate; EB=ethidium bromide; EM=erythromycin; FA=fatty acids; FQ=fluoroquinolones; FU=fusidic acid; GM=gentamicin; INH=isoniazid; LC=lincosamides; LZ=linezolid; MB=methylene blue; MC=macrolides; MD=metronidazole; MI= minocycline; MP=meropenem; MS=metal salts; NA=nalidixic acid; NF=norfloxacin; NO=novobiocin; NT=nitrofurantoin OQ=olaquindox; OS=organic solvents; PH=Phloretin; PM=polymyxin B; PR=pristinamycin; PY=pyronine; RF=rifampin; RG=rhodamine 6G; SAM= ampicillin-sulbactam; SDS=sodium dodecyl sulphate; SA=safranin; SF=sulfonamides; SM=streptomycin; SXT=trimethoprim sulfamethoxazole; TC=tetracyclines; TF=toxoflavin; TG=tigecycline; TM=trimethoprim; TP=thiamphenicol; TPP=tetraphenylphosphonium; TR=triclosan; TT=tributyltin; VC=vancomycin; ?=the efflux components or regulators remain unknown or no genes linked to the transporter structural gene(s) are identified.