Aquatic Environments as Hotspots of Transferable Low-Level Quinolone Resistance and Their Potential Contribution to High-Level Quinolone Resistance
Abstract
:1. Introduction
2. Quinolone Residues in Aquatic Environments
3. Mechanisms of Quinolone Resistance
3.1. High-Level Resistance to Quinolones
3.2. Acquired Low-Level Resistance to Quinolones
4. Quinolone Resistance Genes (qnr)
4.1. Origin and Structure of qnr Genes
4.2. Antimicrobial Activity of qnr Genes
Gene | MIC (µg/mL) | Reference | |||
---|---|---|---|---|---|
CIP | LVX | NFX | NAL | ||
qnrA | 0.125 (0.002) | 0.5 (0.008) | 0.5 (0.015) | NT | [149] |
0.125 (0.002) | NT | 0.25 (0.015) | 8 (2) | [144] | |
0.125 (0.002) | 0.5 (0.008) | NT | NT | [121] | |
0.25 (0.008) | 0.5 (0.015) | NT | 16 (4) | [87] | |
0.125 (0.002) | 0.125 (0.004) | NT | NT | [163] | |
0.25 (0.008) | 0.5 (0.015) | NT | 16 (4) | [109] | |
0.25 (0.008) | NT | NT | NT | [164] | |
qnrB | 0.125 (0.002) | 0.125 (0.008) | 0.25 (0.015) | NT | [149] |
0.125 (0.002) | 0.125 (0.008) | NT | NT | [121] | |
0.25 (0.008) | 0.5 (0.015) | NT | 16 (4) | [87] | |
0.06 (0.002) | NT | NT | 8 (2) | [150] | |
0.25 (0.008) | 0.5 (0.015) | NT | 16 (4) | [109] | |
qnrC | 0.25 (0.008) | 0.25 (0.015) | NT | 16 (4) | [109] |
qnrD | 0.06 (0.002) | NT | 0.06 (0.015) | 4 (2) | [144] |
0.06 (0.008) | NT | NT | 4 (4) | [109] | |
qnrE | 0.125 (0.002) | 0.125 (0.004) | NT | 8 (1) | [148] |
qnrS | 0.125 (0.002) | 0.5 (0.008) | 0.5 (0.015) | NT | [149] |
0.06 (0.002) | NT | 0.06 (0.015) | 4 (2) | [144] | |
0.125 (0.002) | 0.5 (0.008) | NT | NT | [121] | |
0.25 (0.008) | 0.38 (0.015) | NT | 16 (4) | [87] | |
0.25 (0.008) | 0.38 (0.015) | NT | 16 (4) | [109] | |
0.25 (<0.01) | NT | 1 (0.03) | 4 (1) | [165] | |
qnrVC | 0.5 (0.0075) | NT | NT | 16 (0.12) | [166] |
0.5 (0.125) | NT | 4 (1) | 400 (50) | [156] | |
0.25 (0.125) | NT | 2 (1) | 200 (50) | [156] | |
E. coli SBV | ≤1 | ≤2 | NT | ≤16 | [167] |
4.3. Occurrence of qnr Genes in Aquatic Environments
4.4. Prevalence and Spread of qnr Genes in Aquatic Environments
4.5. Role of qnr Genes in the Acquisition of High-Level Resistance
5. Conclusions
6. Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
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Sample | Source | Mean or Range of Quinolones (ng/L or µg/kg) | Reference | |||
---|---|---|---|---|---|---|
OFX | NFX | CIP | ENR | |||
Water | Suquía River, Argentina | nd–69 | nd–80 | nd–78 | NT | [26] |
Southeast Queensland, Australia | NT | 1,150 | 300 | 1300 | [27] | |
Belém River, Brazil | NT | 110 | <20 | NT | [28] | |
Barigui River, Brazil | NT | <20–130 | 70 | NT | [28] | |
Hunhe River, China | nd–280 | nd–1380 | nd–65 | nd–17 | [29] | |
Bohai Sea, China | 3–5100 | 32–6800 | 4.9–390 | NT | [30] | |
Haihe River, China | 180 | NT | 130 | NT | [31] | |
Baiyangdian Lake, China | 0.38–32.6 | nd–156 | nd–60.3 | nd–4.42 | [32] | |
Laizhou Bay, China | nd–45.5 | nd–572 | nd–346 | nd–24.6 | [33] | |
Xiaoqing River, China | 9.5–1605 | nd | nd–56.6 | nd | [34] | |
Huangpu River, China | nd–6.5 | nd–2.6 | nd–2.7 | nd | [35] | |
Tai Lake, China | 14–474 | 59–271 | 18–269 | 19–229 | [36] | |
Pearl River, China | 7.1 | 67.5 | NT | nd | [37] | |
Victoria Harbor, China | 660–6840 | 14–2290 | NT | NT | [38] | |
River, Beijing, China | 663.9–2722 | NT | NT | NT | [39] | |
Huangpu River, China | nd–28.5 | nd–0.2 | nd–34.2 | nd–14.6 | [40] | |
Yangjie River, China | 0.14–4.49 | 0.11–2.37 | 0.77–4.32 | 0.53 5.56 | [41] | |
Danjiangkou Reservoir, China | 2.0–2.9 | 0.55–0.61 | 0.87–1.1 | 0.81 1.2 | [42] | |
Liuxi River, China | NT | 7.06 | NT | NT | [43] | |
Zhujiang River, China | NT | 4.85 | NT | NT | [43] | |
Shijing River, China | NT | 70.4 | NT | NT | [43] | |
Pearl River Delta, China | NT | 4.14–6.62 | NT | NT | [44] | |
Qingshitan Reservoir, China | 50.0–660.13 | 3.70–3.49 | 3.49–6.22 | 4.59–6.06 | [45] | |
Musi River, India | 1553.0–542,452.0 | 16,148.0–251,137.0 | 7447.0–5015.7 | 2262.0–181,609.0 | [46] | |
Kshipra River, India | 640–1460 | nd–980 | nd | NT | [47] | |
Kan River, Iran | NT | NT | 9.87 | NT | [48] | |
Firozabad Ditch, Iran | NT | NT | 212.83 | NT | [48] | |
Po River, Italy | 0.65–18.06 | NT | 1.32–16 | NT | [49] | |
Arno River, Italy | <1.4–10.88 | NT | <1.8–37.5 | NT | [49] | |
Lambro River, Italy | 306 | NT | 26,200 | NT | [50] | |
River and Estuaries, Osaka, Japan | nd–510 | nd–33 | 2.6–37 | nd–4.4 | [51] | |
Mitheu River, Kenya | NT | 600–2200 | 500–1300 | NT | [52] | |
Sagana River, Kenya | NT | nd | 200 | NT | [52] | |
Chania River, Kenya | NT | 100–2600 | nd | NT | [52] | |
Mwania River, Kenya | NT | 110 | 500 | NT | [52] | |
Kanyuru River, Kenya | NT | nd | 200 | NT | [52] | |
Douro River, Portugal | nd | NT | nd | NT | [53] | |
Leça River, Portugal | 120 | NT | 339 | NT | [53] | |
Titicaca Lake, Perú | NT | NT | 85.5–652.7 | 56.2–63.0 | [54] | |
East Aurora, USA | NT | NT | nd–360 | NT | [55] | |
Sediment | Suquía River, Argentina | nd–39 | nd | NT | NT | [26] |
Jiaozhou Bay, China | nd–33.83 | NT | nd–11.52 | nd–1.92 | [56] | |
Yellow River, China | 3.07 | 8.34 | 32.8 | nd | [31] | |
Haihe River, China | 10.3 | 32 | 16 | nd | [31] | |
Liaohe River, China | 3.56 | 3.32 | Nd | nd | [31] | |
Qinghe River, China | 5.9 | 49.1 | 28.3 | 2.2 | [57] | |
Huangpu River, China | nd–12.4 | NT | nd–3.2 | NT | [40] | |
Danjiangkou Reservoir, China | 1.2–1.9 | 1.7–2 | 0.98–1.1 | 1.2–1.3 | [42] | |
Pearl River Estuary, China | nd–2.08 | 50.24–153.06 | NT | nd–25.62 | [37] | |
Pearl River Delta, China | NT | 1.88–11.20 | 0.76–2.42 | NT | [44] | |
Qingshitan Reservoir, China | 1.03–118.11 | 20.17–722.18 | 17.48–557.18 | 4.70–331.82 | [45] | |
Charmoise River, France | 4.9–603 | 1.6–225 | 2.9–569 | 6.6–11 | [58] | |
Patancheru River, India | nd–3545 * | nd | 449–914,044 * | 374–102,865 * | [59] | |
Musi River, India | 890.0–444,916.0 | nd–232,918.0 | nd–3316.5 | 4471.0–721,491.0 | [46] | |
Nakkavagu River, India | 0.63 | 0.14 | 10 | 0.064 | [60] | |
Isakavagu River, India | 0.91 | 0.68 | 12 | nd | [60] | |
Mitheu River, Kenya | NT | nd | 29.3 | NT | [52] | |
Sagana River, Kenya | NT | nd | nd | NT | [52] | |
Chania River, Kenya | NT | 26.6 | nd | NT | [52] | |
Kanyuru River, Kenya | NT | nd | 47.4 | NT | [52] | |
Titicaca Lake, Perú | NT | NT | 950–3010 | 150–3740 | [54] | |
Grifn Lake, Switzerland | NT | 2.4 | 2.52 | NT | [61] | |
Northwest River, USA | <21 | NT | <10 | NT | [62] | |
Fish | Guangdong, China | NT | 46.64–106.85 | 27.07–165.15 | 1.0–34.20 | [63] |
Guiyang, China | nd–385.73 | nd | nd–16.37 | 0.30–312.00 | [64] | |
Hongze Lake, China | NT | NT | 15.0–24.0 | NT | [65] | |
Jining, China | NT | NT | 2.08–33.8 | nd–3.25 | [66] | |
Suzhou, China | nd–4.35 | NT | nd–33.7 | 3.7–90.6 | [33] | |
Pearl River Delta, China | NT | 1.95–43.51 | 1.03–2.16 | 0.65–1.71 | [44] | |
Qingshitan Reservoir, China | 58.59–968.66 | 9.15–33.27 | 12.15–80.26 | 6.73–102.87 | [45] | |
Titicaca Lake, Perú | NT | NT | 3.4–3.9 | 3.8–4.8 | [54] |
Gene | Percentage of Nuleotide/Amino Acid Similarity (%) | ||||||
---|---|---|---|---|---|---|---|
qnrA | qnrB | qnrC | qnrD | qnrE | qnrS | qnrVC | |
qnrA | 100/100 | 46.33/41.59 | 59.36/64.22 | 47.91/46.26 | 48.99/42.06 | 58.75/59.63 | 60.43/61.93 |
qnrB | 100/100 | 48.78/42.99 | 62.79/64.49 | 75.81/85.98 | 48.32/39.72 | 50/42.99 | |
qnrC | 100/100 | 49.77/44.39 | 46.98/42.52 | 60.73/60.09 | 68.65/73.85 | ||
qnrD | 100/100 | 63.10/65.89 | 46.51/39.25 | 50.70/43.93 | |||
qnrE | 100/100 | 48.37/35.98 | 49.61/42.06 | ||||
qnrS | 100/100 | 63.93/64.68 | |||||
qnrVC | 100/100 |
Environment | Country | Source | Species Carrying a qnr Gene | Location | Reference |
---|---|---|---|---|---|
Freshwater | Bangladesh | Water | qnrB, qnrS: Eschericia coli | ND | [172] |
Belgium | Water | qnrS: ND | ND | [173] | |
Brazil | Water | qnrB, qnrS: Klebsiella pneumonia | ND | [174] | |
Brazil | River Water/Sediment | qnrB, qnrS: ND | ND | [175] | |
Canada | Wastewater/River Water | qnrS: ND | ND | [176] | |
Canada, China, Sri Lanka, South Korea, USA | Fish | qnrA: Aeromonas hydrophila | ND | [177] | |
Chile | Reared fish | qnrB: Citrobacter gillenii | ND | [151] | |
China | Fish | qnrB, qnrD, qnrS: Escherichia coli | Pl (qnrS), ND | [178] | |
China | Fish | qnrA, qnrS: Aeromonas spp. | ND | [179] | |
China | Fish/River Water | qnrA, qnrB, qnrS: ND | ND | [180] | |
China | Water | qnrD, qnrS: ND | ND | [181] | |
China | Water/Sediment | qnrS: ND | ND | [182] | |
China | River Water/Sediment | qnrB, qnrS: ND | ND | [183] | |
Water | qnrS: ND | ND | [184] | ||
China | River Water/Sediment | qnrA, qnrS: ND | ND | [185] | |
China | Water | qnrB: Klebsiella pneumoniae, Raoultella omithinolytica.; qnrS: Aeromonas caviae, Aeromonas hydrophila, Aeromonas allosaccharophila, Aeromonas veronii, Escherichia coli, Klebsiella pneumoniae, Enterobacter hormaechei, Leclercia adecarboxylata, Enterococcus faecalis | Pl (qnrS), ND | [186] | |
China | Fish/Shrimp | qnrA, qnrD: ND | ND | [13] | |
China | Shrimp | qnrD: ND | Pl | [187] | |
China | Shrimp | qnrA: ND | ND | [188] | |
China | River Water | qnrS: ND | ND | [189] | |
China | Lake Water | qnrA, qnrB, qnrD, qnrS: ND | ND | [190] | |
China | Lake Water | qnrA, qnrB, qnrD, qnrS: ND | ND | [191] | |
China | Wastewater/River Water | qnrA: Enterobacter sp., Proteus sp., Citrobacter sp.; qnrB: Klebsiella sp., Enterobacter sp., Proteus sp., Shigella sp., Citrobacter sp. qnrS: Klebsiella sp., Escherichia coli, Enterobacter sp.; | Pl, Cr | [192] | |
China | Wastewater/River Water | qnrC, qnrD: ND | Pl | [39] | |
China | Wastewater/River Water | qnrA, qnrB, qnrS: ND | ND | [193] | |
China | Eel, Pond Water | qnrA, qnrB, qnrS: ND | ND | [194] | |
China | Water | qnrB: Salmonella typhi, Salmonella enteriditis, Salmonella typhimurium | ND | [195] | |
China | River Water/Sediment | qnrA, qnrB, qnrD, qnrS: ND | ND | [196] | |
China | River Water | qnrD: ND | ND | [197] | |
China | Water | qnrS: ND | ND | [198] | |
China | Water | qnrA, qnrD, qnrS: ND | ND | [199] | |
China | Water | qnrB, qnrS: Escherichia coli | Pl | [200] | |
China | Water | qnrD, qnrS: ND | ND | [201] | |
China | River Water | qnrD, qnrS: ND | ND | [202] | |
China | River Water/Sediment | qnrA: ND | ND | [203] | |
China | Water/Sediment | qnrA, qnrB, qnrD, qnrS: ND | ND | [204] | |
Egypt | Fish | qnrA, qnrB, qnrS: Edwarsiella tarda | ND | [205] | |
France | Water | qnrS: Aeromonas punctata, Aeromonas media | Pl | [206] | |
India | Fish | qnrS: Aeromonas hydrophila | Pl | [207] | |
India | Sediment | qnrB, qnrD, qnrS, qnrVC: ND | ND | [69] | |
India | River Sediment | qnrS: ND | ND | [208] | |
India | River Water | qnrD, qnrS, qnrVC: ND | ND | [59] | |
India | Water | qnrS: Acinetobacter sp., Pseudomonas sp., Aeromonas sp., Brevibacterium frigoritolerans | Pl | [209] | |
India | Water/Sediment | qnrA, qnrB: ND | ND | [210] | |
India, Sri Lanka | Water | qnrS: ND | ND | [211] | |
Iran | Water | qnrA, qnrB, qnrS: Escherichia coli | ND | [212] | |
Iraq | Water | qnrA: Escherichia coli | ND | [213] | |
Ireland | River Water | qnrS: ND | ND | [214] | |
Italy | River Water | qnrS: ND | ND | [215] | |
Italy | Water | qnrS: ND | ND | [216] | |
Italy | River Water | qnrS: ND | ND | [217] | |
Italy | River Water | qnrS: ND | ND | [218] | |
Japan | River Water | qnrS: Escherichia coli | Pl | [51] | |
Korea | Fish | qnrS: Aeromonas sp. | Pl | [219] | |
Mexico | Sediment | qnrB: ND | Pl | [220] | |
Mexico, USA | Sediment | qnrA, qnrB, qnrS: ND | ND | [221] | |
Poland | Water | qnrD: Eschericia coli, Acinetobacter sp., Acinetobacter johnsonii, Acinetobacter guillouiae, Aeromonas sp., Bacillus sp., Pseudomonas sp., Cronobacter sp., Acidovorax sp., Hydrogenophaga sp., Kurthia sp., Providencia sp., Psychrobacter sp., Shigella sp., Vibrio sp. qnrS: Sphingobacterium sp., Pedobacter sp., Eschericia coli, Acinetobacter sp., Acinetobacter johnsonii, Aeromonas sp., Bacillus sp, Kurthia sp., Shigella sp. | Pl | [222] | |
Portugal | Water | qnrA: Escherichia coli | ND | [223] | |
Portugal | Water | qnrS: ND | ND | [224] | |
Portugal | Water | qnrA, qnrB, qnrS: ND | ND | [225] | |
Portugal | Water | qnrVC: Aeromonas hydrophila, Pseudomonas sp., Escherichia coli, Aeromonas sp. | ND | [226] | |
Spain | Biofilm | qnrB: Klebsiella oxytoca; qnrS: Aeromonas sp. | Pl | [227] | |
Spain | Biofilm | qnrS: ND | ND | [228] | |
Spain | Sediment | qnrB: Citrobacter freundii; qnrS: Aeromonas sp., Raoutella terrígena | Pl | [227] | |
Spain | Sediment | qnrS: ND | ND | [229] | |
Spain | River Water | qnrS: ND | ND | [230] | |
Spain | Sediment | qnrB: Escherichia coli, Raoultella ornithinolytica, Enterobacter cloacae | Pl | [231] | |
Spain | Water | qnrS: ND | ND | [22] | |
Spain | Water | qnrS: ND | ND | [232] | |
Spain | Water | qnrA, qnrS: ND | ND | [233] | |
Spain | Water | qnrS: ND | ND | [234] | |
Spain | Water/Sediment | qnrA, qnrS: ND | ND | [235] | |
South Africa | Fish | qnrB: Aeromonas veronii, Aeromonas caviae, Aeromonas hydrophila, Aeromonas jandaei qnrS: Aeromonas veronii, Aeromonas hydrophila, Aeromonas jandaei | ND | [236] | |
Switzerland | Lake Water | qnrS: Aeromonas allosaccharophila | Pl | [164] | |
Switzerland | Water | qnrS: Escherichia coli | Pl | [237] | |
Thailand | Shrimp/Pond Water | qnrVC: Vibrio parahaemolyticus | ND | [238] | |
Thailand and Vietnam | Water | qnrB: Brevundimonas diminuta, Blastobacter aggregatus, Janibacter anophelis; qnrS: Escherichia coli | ND | [239] | |
United Kingdom | River Water | qnrS: ND | ND | [240] | |
United Kingdom | River Water | qnrS: ND | ND | [241] | |
United States | River Water | qnrA: ND | ND | [242] | |
Seawater | Antarctica | Sediment | qnrS: ND | ND | [243] |
Australia | Water | qnrS: ND | ND | [244] | |
Brazil | Water/Sand | qnrA, qnrB, qnrS: ND | ND | [245] | |
Chile | Water/Sediment | qnrA: Alcanivorax sp., Arcobacter sp., Arthrobacter sp., Kytococcus sp., Marinobacter sp., Microbacterium sp., Pseudomonas sp., Rhodococcus sp.; qnrB: Kytococcus sp., Marinobacter sp., Rhodococcus sp., Actinobacterium sp., Cellulophaga sp., Flavobacteriaceae, Erythrobacter sp., Tsukamurella sp.; Rhodococcus sp.; Marinobacter sp.; Kylococcus sp.; qnrS: Arcobacter sp., Arthrobacter sp., Marinobacter sp., Pseudomonas sp., Rhodococcus sp., Cellulophaga sp., Erythrobacter sp., Dietzia sp., Microbacter sp. | Pl, Cr | [246,247] | |
China | Fish | qnrA, qnrC: ND | ND | [178] | |
China | Sediment | qnrA: Escherichia coli, Proteus mirabilis, Providencia stuartii, Klebsiella pneumoniae | Pl, ND | [248] | |
China | Sediment | qnrS: ND | ND | [249] | |
China | Fish | qnrA, qnrB, qnrD, qnrS: ND | ND | [250] | |
China | Sediment | qnrA,qnrB,qnrD,qnrS: ND | ND | [251] | |
China | Water/Sediment | qnrB,qnrS: ND | ND | [252] | |
China | Water | qnrA: Shewanella algae; qnrB: Citrobacter freundii; qnrD: Proteus vulgaris; qnrS: Enterobacter sp., Klebsiella pneumoniae, Pseudoalteromonas sp., Pseudomonas sp. | Pl, Cr | [253] | |
China | Water/Sediment | qnrS: ND | ND | [254] | |
Egypt | Water | qnrA: Klebsiella pneumoniae, Enterobacter cloacae, Citrobacter koseri, Proteus mirabilis, Shewanella putrefaciens; qnrB: Klebsiella pneumoniae, Citrobacter koseri, qnrS: Klebsiella pneumoniae, Aeromonas hydrophila, Enterobacter cloacae, Escherichia coli, Citrobacter sp., Pasteurella sp. | ND | [255] | |
Italy | Water | qnrS: ND | ND | [216] | |
Italy | Water/Sediment | qnrA: Shewanella algae; qnrVC: Vibrio anguillarum | Pl | [256] | |
Portugal | Fish | qnrB: Leclercia adecarboxylata | ND | [257] | |
Portugal | Clams/Oysters | qnrA, qnrB, qnrS: ND | Pl | [258] | |
Singapore | Water/Sediment | qnrA: ND | ND | [259] | |
South Korea | Fish Farm Effluent | qnrS: ND | Pl | [260] | |
South Korea | Fish Farm Effluent | qnrD: Psychrosphaera; qnrS: ND | ND | [261] | |
Turkey | Fish | qnrS: Pantoea agglomerans | ND | [262] | |
United States | Fish | qnrS: Vibrio sp. | ND | [263] |
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Miranda, C.D.; Concha, C.; Godoy, F.A.; Lee, M.R. Aquatic Environments as Hotspots of Transferable Low-Level Quinolone Resistance and Their Potential Contribution to High-Level Quinolone Resistance. Antibiotics 2022, 11, 1487. https://doi.org/10.3390/antibiotics11111487
Miranda CD, Concha C, Godoy FA, Lee MR. Aquatic Environments as Hotspots of Transferable Low-Level Quinolone Resistance and Their Potential Contribution to High-Level Quinolone Resistance. Antibiotics. 2022; 11(11):1487. https://doi.org/10.3390/antibiotics11111487
Chicago/Turabian StyleMiranda, Claudio D., Christopher Concha, Félix A. Godoy, and Matthew R. Lee. 2022. "Aquatic Environments as Hotspots of Transferable Low-Level Quinolone Resistance and Their Potential Contribution to High-Level Quinolone Resistance" Antibiotics 11, no. 11: 1487. https://doi.org/10.3390/antibiotics11111487
APA StyleMiranda, C. D., Concha, C., Godoy, F. A., & Lee, M. R. (2022). Aquatic Environments as Hotspots of Transferable Low-Level Quinolone Resistance and Their Potential Contribution to High-Level Quinolone Resistance. Antibiotics, 11(11), 1487. https://doi.org/10.3390/antibiotics11111487