Abstract
The use of dietary polyphenols as antimicrobial agents has gained immense popularity in recent years, although few of them—like tannic acid has limited use in this field of research; one of the main reasons is its restricted access through the bacterial membrane. Dissipating the bacterial membrane potential with a sub-lethal dosage of the protonophore, carbonyl cyanide m-chlorophenyl hydrazone, enhanced the tannic acid-cytotoxicity with subsequent inhibition of aerobic respiration in Pseudomonas aeruginosa strains which otherwise exhibited a minimum response to tannic acid. However, ascorbic acid, an antioxidant and bacterial membrane-stabilizing compound, had rescued the cells from both tannic acid- and CCCP-mediated lethality. The results suggested that dispersing the membrane potential with a protonophore can enhance the antibacterial properties of tannic acid.
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Abbreviations
- CCCP:
-
Carbonyl cyanide m-chlorophenyl hydrazine
- AA:
-
Ascorbic acid
- TA:
-
Tannic acid
- GA:
-
Gallic acid
- OCR:
-
Oxygen consumption rate
- Disc3(5):
-
3,3’-dipropylthiadicarbocyanine iodide
References
Bassetti M, Vena A, Croxatto A et al (2018) How to manage Pseudomonas aeruginosa infections. Drugs Context 7:212527. https://doi.org/10.7573/dic.212527dic-7-212527
Pachori P, Gothalwal R, Gandhi P (2019) Emergence of antibiotic resistance Pseudomonas aeruginosa in intensive care unit; a critical review. Genes Dis 6:109–119. https://doi.org/10.1016/j.gendis.2019.04.001
Adewunmi Y, Namjilsuren S, Walker WD et al (2020) antimicrobial activity of, and cellular pathways targeted by, p-anisaldehyde and epigallocatechin gallate in the opportunistic human pathogen Pseudomonas aeruginosa. Appl Environ Microbiol. https://doi.org/10.1128/AEM.02482-19
Kosuru RY, Aashique M, Fathima A et al (2018) Revealing the dual role of gallic acid in modulating ampicillin sensitivity of Pseudomonas aeruginosa biofilms. Future Microbiol 13:297–312. https://doi.org/10.2217/fmb-2017-0132
Zhou JW, Chen TT, Tan XJ et al (2018) Can the quorum sensing inhibitor resveratrol function as an aminoglycoside antibiotic accelerant against Pseudomonas aeruginosa? Int J Antimicrob Agents 52:35–41. https://doi.org/10.1016/j.ijantimicag.2018.03.002
Chen T, Sheng J, Fu Y et al (2017) (1)H NMR-based global metabolic studies of pseudomonas aeruginosa upon exposure of the quorum sensing inhibitor resveratrol. J Proteome Res 16:824–830. https://doi.org/10.1021/acs.jproteome.6b00800
Kanagaratnam R, Sheikh R, Alharbi F, Kwon DH (2017) An efflux pump (MexAB-OprM) of Pseudomonas aeruginosa is associated with antibacterial activity of Epigallocatechin-3-gallate (EGCG). Phytomedicine 36:194–200. https://doi.org/10.1016/j.phymed.2017.10.010
Sahiner N, Sagbas S, Sahiner M et al (2016) Biocompatible and biodegradable poly(Tannic Acid) hydrogel with antimicrobial and antioxidant properties. Int J Biol Macromol 82:150–159. https://doi.org/10.1016/j.ijbiomac.2015.10.057
Schestakow A, Hannig M (2020) Effects of experimental agents containing tannic acid or chitosan on the bacterial biofilm formation in situ. Biomolecules. https://doi.org/10.3390/biom10091315
Huang Q, Liu X, Zhao G et al (2018) Potential and challenges of tannins as an alternative to in-feed antibiotics for farm animal production. Animal Nutr 4:137–150. https://doi.org/10.1016/j.aninu.2017.09.004
Murata W, Tanaka T, Kubo I, Fujita K (2013) Protective effects of alpha-tocopherol and ascorbic acid against cardol-induced cell death and reactive oxygen species generation in Staphylococcus aureus. Planta Med 79:768–74. https://doi.org/10.1055/s-0032-1328555
Sorice A, Guerriero E, Capone F et al (2014) Ascorbic acid: its role in immune system and chronic inflammation diseases. Mini Rev Med Chem 14:444–52. https://doi.org/10.2174/1389557514666140428112602
Mousavi S, Bereswill S, Heimesaat MM (2019) Immunomodulatory and antimicrobial effects of Vitamin C. Eur J Microbiol Immunol (Bp) 9:73–79. https://doi.org/10.1556/1886.2019.00016
Chung KT, Wong TY, Wei CI et al (1998) Tannins and human health: a review. Crit Rev Food Sci Nutr 38:421–64. https://doi.org/10.1080/10408699891274273
Kırmusaoğlu S (2019) Sensitizing of β-lactam resistance by tannic acid in methicillin-resistant S aureus. World J Microbiol Biotechnol. https://doi.org/10.1007/s11274-019-2637-6
Sahiner N, Sagbas S, Aktas N, Silan C (2016) Inherently antioxidant and antimicrobial tannic acid release from poly(tannic acid) nanoparticles with controllable degradability. Colloids Surf B Biointerfaces 142:334–343. https://doi.org/10.1016/j.colsurfb.2016.03.006
Tintino SR, Oliveira-Tintino CD, Campina FF et al (2016) Evaluation of the tannic acid inhibitory effect against the NorA efflux pump of Staphylococcus aureus. Microb Pathog 97:9–13. https://doi.org/10.1016/j.micpath.2016.04.003
Wu D, Wu XD, You XF et al (2010) Inhibitory effects on bacterial growth and beta-ketoacyl-ACP reductase by different species of maple leaf extracts and tannic acid. Phytother Res 24(Suppl 1):S35-41. https://doi.org/10.1002/ptr.2873
Chung KT, Lu Z, Chou MW (1998) Mechanism of inhibition of tannic acid and related compounds on the growth of intestinal bacteria. Food Chem Toxicol 36:1053–60. https://doi.org/10.1016/s0278-6915(98)00086-6
Dong G, Liu H, Yu X et al (2018) Antimicrobial and anti-biofilm activity of tannic acid against Staphylococcus aureus. Nat Prod Res 32:2225–2228. https://doi.org/10.1080/14786419.2017.1366485
Kim S, Chen J, Cheng T et al (2019) PubChem 2019 update: improved access to chemical data. Nucleic Acids Res 47:D1102–D1109. https://doi.org/10.1093/nar/gky10335146201
Fass RJ, Barnishan J (1979) Minimal inhibitory concentrations of 34 antimicrobial agents for control strains Escherichia coli ATCC 25922 and Pseudomonas aeruginosa ATCC 27853. Antimicrob Agents Chemother 16:622–4. https://doi.org/10.1128/aac.16.5.622
Blanco P, Hernando-Amado S, Reales-Calderon JA et al (2016) Bacterial multidrug efflux pumps: much more than antibiotic resistance determinants. Microorganisms. https://doi.org/10.3390/microorganisms4010014
Valderrama K, Pradel E, Firsov AM et al (2019) Pyrrolomycins are potent natural protonophores. Antimicrob Agents Chemother. https://doi.org/10.1128/AAC.01450-19
Sezikli M, Guzelbulut F, Akkan Cetinkaya Z (2016) Influence of vitamin C and E supplementation on the eradication rates of triple and quadruple eradication regimens in Helicobacter pylori infection. Turk J Gastroenterol 27:290–1. https://doi.org/10.5152/tjg.2016.16105
Helgadóttir S, Pandit S, Mokkapati VRSS et al (2017) Vitamin C pretreatment enhances the antibacterial effect of cold atmospheric plasma. Front Cell Infect Microbiol 7:43. https://doi.org/10.3389/fcimb.2017.00043
Syal K, Chatterji D (2018) Vitamin C: A Natural Inhibitor of Cell Wall Functions and Stress Response in Mycobacteria. In: Chattopadhyay K, Basu SC (eds) Biochemical and Biophysical Roles of Cell Surface Molecules. Springer Singapore, Singapore, pp 321–332
El-Mowafy SA, Shaaban MI, Abd El Galil KH (2014) Sodium ascorbate as a quorum sensing inhibitor of Pseudomonas aeruginosa. J Appl Microbiol 117:1388–99. https://doi.org/10.1111/jam.12631
Pandit S, Ravikumar V, Abdel-Haleem AM et al (2017) Low Concentrations of Vitamin C reduce the synthesis of extracellular polymers and destabilize bacterial biofilms. Front Microbiol 8:2599. https://doi.org/10.3389/fmicb.2017.02599
Funding
This work was supported by research grants from the Department of Biotechnology, Govt. of India (Ref. 6242-P5/RGCB/PMD/DBT/SMNB/2015) to SB, from the Science and Engineering Research Board, Department of Science and Technology, Govt. of India (Ref. ECR/2016/000898) to AR, and Institutional research fellowship to RY.
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MA has conceptualized the work, designed and conducted the experiments, analyzed the data, and prepared the manuscript; AR has conceptualized the work and prepared the manuscript, RY has designed and conducted the experiments, and analyzed the data; SB has conceptualized the work, designed the experiments, prepared the manuscript, and supervised the overall work.
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Aashique, M., Roy, A., Kosuru, R.Y. et al. Membrane Depolarization Sensitizes Pseudomonas aeruginosa Against Tannic Acid. Curr Microbiol 78, 713–717 (2021). https://doi.org/10.1007/s00284-020-02330-7
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DOI: https://doi.org/10.1007/s00284-020-02330-7