Table 1. List of Characterized Tripartite Systems in Gram-Negative Bacteria and Their Substrate Profilesa.
Microorganism | Efflux pump family | Efflux system | Substrates | refs |
---|---|---|---|---|
Acinetobacter baumannii | RND | AdeABC | AG, BL, CHL, CHX, ML, FA, FQ, TET, TGC, TMP | (11, 19, 20) |
AdeFGH | CHL, FQ, SUL, TET, TGC, TMP | (21) | ||
AdeIJK | BL, CHL, CHX, ERY, FA, FQ, NOV, TET, TGC, TMP, TRI | (11) | ||
AbuO | AG, BL, TGC | (22) | ||
ArpAB | AG | (23) | ||
ABC | MacAB-TolC | ML | (24) | |
Acinetobacter Genomic DNA Group 3 | RND | AdeDE | CHL, FQ, TET | (25, 26) |
AdeXYZ | CHL, FQ, BL, TET | (25) | ||
Achromobacter spp. | RND | AxyXY-OprZ | AG, FQ | (27) |
NccABC | Cd2+, Co2+, Ni2+ | (28) | ||
Aeromonas hydrophila | RND | AheABC | RIF | (29) |
Aggregatibacter actinomycetemcomitans | ABC | LtxDB-TolC | LTX | (30) |
Bacteroides fragilis | RND | BmeABC3 | BL, FQ | (31) |
Borrelia burgdorferi | RND | BesABC | ML | (32) |
Bordetella pertussis | ABC | CyaBDE | ACT | (33) |
Bradyrhizobium japonicum | RND | BdeAB-? | AG | (34) |
Brucella suis | RND | BepDE-BepC | ACR, AMP, DOC, EB, FQ, NOV, PMB, SDS, TET | (35) |
BepFG-BepC | DOC, NAL, SDS | (35) | ||
Burkholderia cenocepacia | RND | CeoAB-OpcM | CHL, FQ | (36) |
BCAL2820-BCAL2822 | ATM, AG, CHL, FQ | (37) | ||
Burkholderia pseudomallei | RND | AmrAB-OprA | AG, ML | (38) |
BpeAB-OprB | AG, CHL, ML, TET | (38, 39) | ||
BpeEF-OprC | CHL, TET, TMP | (40) | ||
Burkholderia thailandensis | RND | AmrAB-OprA | AG, ML, TET | (41) |
Campylobacter jejuni | RND | CmeABC | CHL, CTX, ML, FA, FQ, TRI | (42, 43) |
CmeDEF | CTX, FQ, TRI | (44) | ||
Caulobacter crescentus | RND | NczABC | Co2+, Cd2+, Ni2+, Zn2+ | (45) |
Cupriavidus metallidurans | RND | ZneCAB | Zn2+ | (46) |
Dickeya zeae | RND | DesABC | ZMN | (47) |
Enterobacteriaceaeb | RND | AcrAB-TolC | ACR, BAC, BL, CHL, EB, ERY, FA, FQ, NOV, OXN, TET, TGC, TRI, RIF, R6G | (10, 48−50, 52) |
OqxAB-TolCc | CHL, FQ, ML, NIT, TGC | (53) | ||
Escherichia coli | RND | AcrAD-TolC | AG, BL | (54, 55) |
AcrEF-TolC | ACR, BL, CHL, FQs, EB, ERY, R6G, TET, TGC | (10, 56, 57) | ||
MdtEF-TolC | BL, BAC, ML, OXN | (10, 56−58) | ||
CusABC | Ag+, Cu+ | (59) | ||
ABC | MacAB-TolC | ML | (60) | |
HlyBD-TolC | AH | (61) | ||
YhbFGSR- | EB, TET | (62) | ||
TolC | MJ25 | (63) | ||
YojI?-TolC | ||||
MFS | EmrAB-TolC | FQ, NOV, TRI | (10, 56) | |
EmrKY-TolC | TET | (64) | ||
MdtNOP | ACR, PUR | (56) | ||
AaeAB-? | pHBA | (65) | ||
Helicobacter pylori | RND | HefABC | AG, BL, CHL, EB, ERY, FQ, NOV, TET | (66) |
HefDEF | Cd2+, Ni2+, Zn2+ | (67) | ||
Klebsiella aerogenes | RND | EefABC | CHL, BL, ERY, FQ | (68) |
Klebsiella pneumoniae | RND | AcrAB | BAC, BL, ML, FQ, TET, NOV | (69, 70) |
EefABC | BAC, BL, FQ, ERY, TET, NOV | (70) | ||
KexEF | BL, ERY, TET, NOV | (70) | ||
KexD | ML | (71) | ||
KexVWX | BL, NOV | |||
TMexCXD1-TOprJ1c | AG, FQ, TGC | (72) | ||
MFS | KpnGH-TolC | BL, AG, ML | (73) | |
Legionella pneumophila | RND | LpeAB | ML | (74) |
Moraxella catarrhalis | RND | AcrAB-OprM | CTX, ML | (75) |
Neisseria gonorrhoeae | RND | MtrCDE | BL, BS, FQ, ML, TET | (76, 77) |
ABC | MacAB-MtrE | ML | (78) | |
MFS | FarAB-MtrE | FA | (79) | |
Porphyromonas gingivalis | RND | XepCAB | RIF | (80) |
Pseudomonas aeruginosa | RND | MexAB-OprM | AG, BL, CHL, COL, EB, FQ, ML, SDS, SUL, TET, TMP, TRI | (12, 81) |
MexCD-OprJ | BL, CHL, CHX, COL, FQ, ML, QAC, TET, TGC, TMP, TRI | (81) | ||
MexEF-OprN | CHL, FQ, TET, TMP, TRI | (82) | ||
MexGHI-OpmD | ACR, EB, FQ, TET | (83) | ||
MexJK-OprM/OpmH | ERY, TET, TRI | (84) | ||
MexMN-OprM | CHL | (85) | ||
MexPQ-OpmE | ML, FQ | (85) | ||
MexVW-OprM | ACR, CHL, EB, ERY, FQ, TET | (86) | ||
MexXY-OprA/OprM | AG, BL, CHL, FQ, ML, TET, TGC | (81) | ||
MuxABC-OpmB | ATM, ERY, FQ, NOV, TET | (87) | ||
TriABC-OpmH | TRI | (88) | ||
Pseudomonas putida | RND | ArpABC | BL, CHL, ERY, TET | (89) |
MepABC | BL, ERY, TET | (90) | ||
ParXY/TtgC | AG, FQ | (91) | ||
SrpABC | OS | (92) | ||
TtgABC | BL, CHL, ERY, OS, TET | (93) | ||
TtgDEF | OS | (94) | ||
TtgGHI | OS | (95) | ||
Pseudomonas fluorescens | RND | EmhABC | CHL | (96) |
Pseudomonas syringae | RND | PseABC | ACR, ERY, TET | (97) |
Riemerella anatipestifer | RND | RaeABC | AG, SDS | (98) |
RaeEF-RopN | AG, SDS | (99) | ||
Salmonella enterica | RND | AcrAD-TolC | ATM, BL, NOV, SDS | (100) |
AcrEF-TolC | ACR, BAC, BL, CHL, EB, FUS, FQs, NOV, R6G, SDS, TET, TRI | (101) | ||
MdtABC-TolC | NOV | (101) | ||
MdsABC | Au3+, BAC, BL, CHL, NOV | (102) | ||
SilABCc | Ag+ | (103) | ||
ABC | MacAB-TolC | ML | (101) | |
MFS | EmrAB-TolC | NAL, NOV, TRI | (101) | |
Serratia marcescens | RND | SdeAB | CHL, FQ, QAC | (104) |
SdeGH | FQ | (105) | ||
SdePQ | FQ | (105) | ||
SdeXY-HasF | BAC, CHL, CHX, FQ, ML, QAC, TET, TGC, TRI | (106, 107) | ||
Sinorhizobium meliloti | RND | SmeAB-TolC | ACR, CHL, ERY, NAL, RIF, SDS, TET | (108) |
SmeCD-TolC | CHL, NAL | (108) | ||
SmeEF-TolC | ERY, TET | (108) | ||
Stenotrophomonas maltophilia | RND | SmeABC | AG, BL, FQ | (109) |
SmeDEF | CHL, FQ, ML, TET, TRI | (110) | ||
SmeGH | BL, CHL, FQ, ML, TET | (109, 111) | ||
SmeIJK | AG, TET | (109) | ||
SmeOP-TolC | AG, FQ, ML, TET | (112) | ||
SmeVWX | CHL, FQ, TET | (113) | ||
SmeYZ | AG, TET | (114) | ||
MFS | EmrCAB | CCCP, NAL | (115) | |
ABC | MacABC | AG, ML, PMB | (116) | |
FuaABC | FUA | (117) | ||
SmaAB | AMK | (118) | ||
SmaCDEF | LEV | (118) | ||
Vibrio cholerae | RND | VexAB- TolC | AMP, ERY, NOV, PEN, PMB, SDS | (119, 120) |
VexCD-TolC | BS, DTG, ERY | (119) | ||
VexEF- TolC | BAC, DOC, EB, ERY, NOR, NOV, SDS, TET, TMP | (119) | ||
VexGH | DTG, NOV | (121) | ||
VexIJK | BS, DTG | (120) | ||
MFS | VceCAB | CCCP, DOC, NAL | (122) | |
Vibrio parahaemolyticus | RND | VmeAB-VpoC | ACR, BL, BS, EB, FQ, ML, NOV, R6G, SDS, TET, TMP | (123) |
VmeCD-VpoC | BAC, BL, BS, ML, NOV, R6G, SDS | (124) | ||
VmeEF-VpoC | BC, EB, NOV, R6G, SDS | (124) | ||
VmeGHI-VpoC | SDS | (124) | ||
VmeTUV-VpoC | ACR, BL, BAC, BC, CHX, EB, R6G, SDS | (124) | ||
VmeYZ-VpoC | BC, NOV, SDS | (124) |
ABC, ATP-binding cassette; ACR, acriflavine; ACT, adenylate cyclase toxin; AG, aminoglycosides; AH, α-hemolysin; AMK, amikacin; AMP, ampicillin; ATM, aztreonam; BAC, benzalkonium chloride; BL, β-lactams; BS, bile salts; CCCP, carbonyl cyanide m-chlorophenylhydrazone; CHL, chloramphenicol; CHX, chlorhexidine; COL, colistin; CTX, cefotaxime; DOC, deoxycholate; DTG, detergents; ERY, erythromycin; EB, ethidium bromide; FA, fatty acids; FUS, fusidic acid; FQ, fluoroquinolones; FUA, fusaric acid; LEV, levofloxacin; LTX, leukotoxin; MFS, major facilitator superfamily; MJ25, microcin J25; ML, macrolides; NAL, nalidixic acid; NIT, nitrofurantoin; NOR, norfloxacin; NOV, novobiocin; OS, organic solvents; OXN, oxazolidinones; PEN, penicillin; pHBA, p-hydroxybenzoic acid; PMB, polymyxin B; PUR, puromycin; QAC, quaternary ammonium compounds; R6G, rhodamine 6G; RIF, rifampicin; RND, resistance-nodulation-division; SDS, sodium dodecyl sulfate; SUL, sulfonamides; TET, tetracycline; TGC, tigecycline; TMP, trimethoprim; TRI, triclosan; ZMN, zeamines.
A large family of Gram-negative bacteria that includes several important pathogenic species such as Citrobacter freundii, Escherichia coli, Klebsiella pneumoniae, Salmonella enterica, and Shigella flexneri.
Pumps that are encoded in plasmids.