Lemon Oils Attenuate the Pathogenicity of Pseudomonas aeruginosa by Quorum Sensing Inhibition
Abstract
:1. Introduction
2. Results
2.1. Chemical Composition
2.2. Virulence Factors Inhibition
2.2.1. Biofilm
2.2.2. Elastase
2.2.3. Pyocyanin
2.2.4. Bacterial Motility
2.2.5. Autoinducer Production
3. Discussion
4. Materials and Methods
4.1. Samples
4.2. Gas Chromatography-Mass Spectrometry
4.3. Strains and Growth Medium
4.4. Bacterial Growth Measurement
4.5. Biofilm Biomass Quantification Assay
4.6. Biofilm Metabolic Activity Assay
4.7. Elastase B Activity and Pyocyanin Quantification
4.8. Swarming and Swimming Motility
4.9. Quantification of N-acyl Homoserine Lactones (AHLs)
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Sample Availability
References
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Compounds | Peak Area (%) | ||||
---|---|---|---|---|---|
RI a | KI b | Lemon Essential Oil | Lemon Terpenes | Lemon Essence | |
Monoterpene hydrocarbons | 91.41 | 91.37 | 87.34 | ||
α-thujene | 932 | 930 | 0.35 | 0.34 | 0.21 |
α-pinene | 940 | 939 | 1.64 | 2.35 | 1.99 |
Camphene | 954 | 954 | 0.05 | 0.04 | 0.05 |
Sabinene | 978 | 975 | 1.76 | 1.58 | 4.39 |
β-pinene | 982 | 979 | 15.41 | 14.20 | 6.68 |
β-myrcene | 995 | 990 | 1.65 | 1.49 | 1.32 |
α-terpinene | 1016 | 1017 | 0.14 | - | - |
p-cymene | 1024 | 1024 | 0.11 | 0.29 | 0.02 |
Allocimene | 1131 | 1132 | - | - | t |
Limonene | 1040 | 1029 | 59.14 | 59.28 | 60.07 |
cis-ocymene | 1046 | 1037 | 0.06 | 0.04 | 0.15 |
trans-ocymene | 1055 | 1050 | 0.10 | 0.08 | - |
γ-terpinene | 1064 | 1059 | 10.48 | 11.05 | 11.57 |
Terpinolene | 1092 | 1088 | 0.54 | 0.64 | 0.88 |
Oxygenated monoterpenes | 5.07 | 4.84 | 8.17 | ||
cis-sabinene hydrate | 1078 | 1070 | 0.09 | 0.10 | - |
trans-sabinene hydrate | 1098 | 1098 | 0.07 | - | - |
Linalool | 1102 | 1095 | 0.18 | 0.24 | 0.29 |
endo-fenchol | 1114 | 1116 | - | - | 0.04 |
cis-p-menth-2-en-1-ol | 1122 | 1121 | - | - | 0.04 |
cis-limonene oxide | 1134 | 1136 | - | 0.02 | 0.01 |
cis-p-mentha-2,8-dien-1-ol | 1136 | 1137 | - | t | t |
trans-limonene oxide | 1139 | 1142 | - | 0.01 | - |
trans-p-menth-2-en-1-ol | 1140 | 1140 | - | - | t |
Camphor | 1144 | 1146 | - | 0.02 | 0.02 |
Camphene hydrate | 1147 | 1149 | - | - | 0.01 |
Citronellal | 1154 | 1153 | 0.10 | 0.13 | - |
Borneol | 1167 | 1169 | - | - | t |
Terpinen-4-ol | 1176 | 1177 | 0.05 | 0.11 | 1.89 |
E-isocitral | 1183 | 1180 | - | - | 0.01 |
α-terpineol | 1189 | 1188 | 0.39 | 0.38 | 1.45 |
Nerol | 1230 | 1229 | 0.02 | 0.02 | 0.14 |
Neral | 1240 | 1238 | 0.01 | 1.09 | 1.17 |
Carvone | 1244 | 1243 | 1.16 | 0.01 | t |
Geraniol | 1258 | 1252 | - | - | 0.07 |
Geranial | 1275 | 1267 | 1.85 | 1.58 | 1.09 |
Isobornyl acetate | 1284 | 1285 | - | 0.01 | t |
Methyl geranate | 1321 | 1324 | - | 0.01 | 0.01 |
trans-carvyl acetate | 1334 | 1342 | - | - | t |
Citronellyl acetate | 1352 | 1352 | 0.03 | 0.04 | 0.07 |
Neryl acetate | 1365 | 1361 | 0.79 | 0.75 | 1.22 |
Geranyl acetate | 1382 | 1381 | 0.30 | 0.30 | 0.58 |
Limonen-10-yl-acetate | 1406 | 1395 | 0.01 | 0.01 | 0.02 |
p-menth-1-en-9-yl acetate | 1415 | 1423 | - | - | t |
Neryl propanoate | 1451 | 1454 | 0.01 | 0.01 | 0.01 |
Geranyl propanoate | 1471 | 1477 | - | 0.01 | 0.01 |
Sesquiterpene hydrocarbons | 2.28 | 1.79 | 3.63 | ||
δ-elemene | 1333 | 1338 | - | t | t |
α-cubebene | 1345 | 1348 | - | - | t |
α-copaene | 1372 | 1376 | - | 0.01 | t |
β-cubebene | 1384 | 1388 | - | t | - |
α-cis-bergamotene | 1410 | 1412 | 0.05 | 0.04 | 0.05 |
β-caryophyllene | 1414 | 1419 | 0.35 | 0.29 | 0.37 |
α-trans-bergamotene | 1433 | 1434 | 0.66 | 0.54 | 0.78 |
cis-β-farnesene | 1438 | 1442 | - | t | t |
α-humulene | 1447 | 1454 | 0.03 | 0.02 | 0.02 |
trans-β-farnesene | 1453 | 1456 | 0.06 | 0.04 | 0.06 |
β-santalene | 1455 | 1459 | 0.02 | 0.02 | 0.02 |
γ-curcumene | 1474 | 1482 | 0.02 | 0.01 | 0.02 |
Valencene | 1486 | 1496 | - | 0.03 | 0.14 |
Bicyclogermacrene | 1489 | 1500 | 0.08 | 0.06 | 1.06 |
trans-α-bisabolene | 1497 | 1507 | 0.08 | 0.06 | 0.11 |
β-bisabolene | 1505 | 1505 | 0.93 | 0.65 | 1.06 |
cis-γ-bisabolene | 1510 | 1515 | 0.01 | 0.01 | 0.02 |
δ-cadinene | 1517 | 1523 | - | 0.01 | 0.01 |
trans-γ-bisabolene | 1526 | 1531 | - | t | 0.01 |
cis- α-bisabolene | 1537 | 1536 | - | 0.01 | 0.02 |
Oxygenated sesquiterpenes | 0.07 | 0.02 | t | ||
Germacrene d-4-ol | 1569 | 1575 | - | t | - |
Spathulenol | 1572 | 1578 | - | t | - |
Caryophyllene oxide | 1574 | 1583 | - | 0.01 | - |
α-bisabolol | 1680 | 1685 | 0.07 | 0.01 | - |
β-bisabolenal | 1759 | 1769 | - | - | t |
Alkanes, aldehydes/ketones and esters | 0.44 | 0.56 | 0.38 | ||
6-methyl-5-hepten-2-one | 990 | 985 | - | 0.02 | - |
Octanal | 1005 | 998 | 0.13 | 0.13 | - |
Octanol | 1079 | 1068 | - | - | 0.04 |
Nonanal | 1106 | 1100 | 0.16 | 0.21 | 0.14 |
Dodecane | 1197 | 1200 | - | 0.01 | - |
Decanal | 1202 | 1201 | 0.08 | 0.11 | 0.12 |
Octanol acetate | 1210 | 1213 | - | 0.01 | - |
Tridecane | 1296 | 1300 | - | t | 0.01 |
Undecanal | 1303 | 1306 | 0.04 | 0.04 | 0.05 |
Nonanyl acetate | 1308 | 1311 | - | t | 0.01 |
Tetradecane | 1395 | 1400 | 0.02 | 0.01 | 0.02 |
Dodecanal | 1403 | 1408 | 0.01 | 0.01 | - |
Hexadecane | 1592 | 1600 | - | t | t |
Tetradecanal | 1604 | 1611 | - | t | - |
Total VOCs | 99.23 | 98.58 | 99.64 |
Samples | P. aeruginosa ATCC 27853 | P. aeruginosa HT5 | ||||||
Control | 0.85 ± 0.04 | 0.74 ± 0.02 | ||||||
Concentration | LEO | LT | LE | Limonene | LEO | LT | LE | Limonene |
4 mg mL−1 | 0.33 ± 0.04 * | 0.31 ± 0.03 * | 0.32 ± 0.03 * | 0.36 ± 0.02 * | 0.28 ± 0.02 * | 0.27 ± 0.02 * | 0.28 ± 0.03 * | 0.30 ± 0.02 * |
2 mg mL−1 | 0.38 ± 0.1 * | 0.36 ± 0.03 * | 0.34 ± 002 * | 0.44 ± 0.02 * | 0.31 ± 0.04 * | 0.29 ± 0,03 * | 0.31 ± 0.04 * | 0.38 ± 0.03 * |
1 mg mL−1 | 0.41 ± 0.03 * | 0.38 ± 0.03 * | 0.37 ± 0.03 * | 0.48 ± 0.02 * | 0.34 ± 0.04 * | 0.36 ± 0.03 * | 0.34 ± 0.03 * | 0.46 ± 0.03 * |
0.5 mg mL−1 | 0.46 ± 0.03 * | 0.42 ± 0.03 * | 0.42 ± 0.02 * | 0.54 ± 0.03 * | 0.37 ± 0.02 * | 0.45 ± 0.04 * | 0.42 ± 0.05 * | 0.53 ± 0.01 * |
0.1 mg mL−1 | 0.52 ± 0.02 * | 0.48 ± 0.02 * | 0.47 ± 0.03 * | 0.65 ± 0.02 * | 0.49 ± 0.03 * | 0.53 ± 0.02 * | 0.47 ± 0.03 * | 0.59 ± 0.03 * |
Samples | P. aeruginosa ATCC 27853 | P. aeruginosa HT5 | ||||||
Control | 21.80 ± 0.03 | 25.20 ± 0.06 | ||||||
Concentration | LEO | LT | LE | Limonene | LEO | LT | LE | Limonene |
4 mg mL−1 | 12.00 ± 0.04 * | 15.0 0 ± 0.04 * | 11.00 ± 0.07 * | 11.00 ± 0.04 * | 17.00 ± 0.06 * | 18.20 ± 0.03 * | 18.10 ± 0.07 * | 17.50 ± 0.05 * |
2 mg mL−1 | 13.90 ± 0.06 * | 15.70 ± 0.03 * | 15.90 ± 0.06 * | 14.20 ± 0.03 * | 17.60 ± 0.02 * | 18.60 ± 0.02 * | 18.20 ± 0.03 * | 18.10 ± 0.04 * |
1 mg mL−1 | 14.90 ± 0.02 * | 16.70 ± 0.03 * | 16.80 ± 0.03 * | 19.50 ± 0.04 * | 18.20 ± 0.03 * | 19.10 ± 0.02 * | 18.90 ± 0.02 * | 19.20 ± 0.03 * |
0.5 mg mL−1 | 16.00 ± 0.04 * | 19.00 ± 0.07 * | 22.30 ± 0.04 | 22.20 ± 0.03 | 18.70 ± 0.03 * | 25.10 ± 0.02 | 25.20 ± 0.06 | 25.40 ± 0.04 |
0.1 mg mL−1 | 16.60 ± 0.04 * | 19.90 ± 0.02 * | 22.60 ± 0.06 | 22.60 ± 0.02 | 19.20 ± 0.03 * | 26.00 ± 0.02 | 26.10 ± 0.02 | 25.80 ± 0.03 |
Samples | P. aeruginosa ATCC 27853 | P. aeruginosa HT5 | ||||||
Control | 14.30 ± 0.05 | 13.00 ± 0.04 | ||||||
Concentration | LEO | LT | LE | Limonene | LEO | LT | LE | Limonene |
4 mg mL−1 | ND | ND | ND | ND | 4.00 ± 0.04 * | 2.90 ± 0.02 * | 5.70 ± 0.05 * | 6.00 ± 0.04 * |
2 mg mL−1 | ND | ND | ND | 2.30 ± 0.05 * | 6.30 ± 0.05 * | 6.50 ± 0.04 * | 8.90 ± 0.02 * | 7.00 ± 0.04 * |
1 mg mL−1 | 2.90 ± 0.04 * | 3.10 ± 0.06 * | 4.20 ± 0.05 * | 5.00 ± 0.04 * | 7.80 ± 0.03 * | 8.10 ± 0.06 * | 9.50 ± 0.04 * | 7.40 ± 0.04 * |
0.5 mg mL−1 | 3.40 ± 0.04 * | 4.20 ± 0.03 * | 5.90 ± 0.04 * | 9.20 ± 0.03 * | 9.00 ± 0.04 * | 8.90 ± 0.06 * | 10.90 ± 0.08 * | 8.90 ± 0.02 * |
0.1 mg mL−1 | 4.20 ± 0.03 * | 5.20 ± 0.03 * | 6.10 ± 0.02 * | 10.26 ± 0.05 * | 11.0 ± 0.07 * | 10.70 ± 0.05 * | 11.00 ± 0.06 * | 11.00 ± 0.07 * |
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Luciardi, M.C.; Blázquez, M.A.; Alberto, M.R.; Cartagena, E.; Arena, M.E. Lemon Oils Attenuate the Pathogenicity of Pseudomonas aeruginosa by Quorum Sensing Inhibition. Molecules 2021, 26, 2863. https://doi.org/10.3390/molecules26102863
Luciardi MC, Blázquez MA, Alberto MR, Cartagena E, Arena ME. Lemon Oils Attenuate the Pathogenicity of Pseudomonas aeruginosa by Quorum Sensing Inhibition. Molecules. 2021; 26(10):2863. https://doi.org/10.3390/molecules26102863
Chicago/Turabian StyleLuciardi, María Constanza, María Amparo Blázquez, María Rosa Alberto, Elena Cartagena, and Mario Eduardo Arena. 2021. "Lemon Oils Attenuate the Pathogenicity of Pseudomonas aeruginosa by Quorum Sensing Inhibition" Molecules 26, no. 10: 2863. https://doi.org/10.3390/molecules26102863