Evaluation of the Defined Bacterial Consortium Efficacy in the Biodegradation of NSAIDs
Abstract
:1. Introduction
2. Results and Discussion
2.1. The Composition and Boundary Conditions for the Action of a Defined Bacterial Consortium
2.1.1. The Qualitative and Quantitative Composition of the Defined Bacterial Consortium
2.1.2. Influence of Temperature and pH
2.1.3. NSAID Degradation in the Presence of Co-Pollutants
2.2. Degradation Studies in an SBR Bioreactor System
3. Materials and Methods
3.1. The Composition and Boundary Conditions for the Action of a Bacterial Consortium
3.2. Assessment of the Qualitative and Quantitative Composition of Microorganisms in Cultures
3.2.1. Fluorescent Labeling of Stenotrophomonas maltophilia KB2 and Pseudomonas moorei KB4 Strains
3.2.2. Fluorescent Labeling of Bacillus thuringiensis B1(2015b) Strain
3.2.3. Selection of a Rifampicin-Resistant Mutant of Planococcus sp. Strain S5
3.3. NSAID Degradation Experiments
3.3.1. Periodic Systems
3.3.2. Bioreactor System
- -
- 1000 mL of activated sludge from the aerated activated sludge chamber (Klimzowiec wastewater treatment plant, Chorzów, Poland);
- -
- 2000 mL of synthetic sewage containing (per 1000 mL): 0.04 g NH4Cl, 0.024 g K2HPO4, 0.008 g KH2PO4, 0.1 g CaCO3, 0.2 g MgSO4 × 7 H2O, 0.04 g NaCl, and 0.005 g iron FeSO4 × 7 H2O [48], which was previously sterilized for 15 min at 121 °C;
- -
- 0.6 mL of 30% glucose solution and ammonium acetate (0.317 g/L) sterilized by microfiltration;
- -
- NSAIDs: 5 mg/L ibuprofen sodium, 10 mg/L paracetamol, 1 mg/L naproxen sodium, and 1 mg/L diclofenac sodium;
- -
- co-contaminants: phenol (1 mM), methanol (1%), and Cu2+ (0.1 mM as Cu(NO3)2);
- -
- supplement: cow’s milk at a concentration of 5% (200 mL of milk per system).
3.4. Biochemical Analysis
3.5. Determination of NSAIDs Concentration
3.6. Statistical Analysis
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Sample Availability
References
- Wojcieszyńska, D.; Guzik, H.; Guzik, U. Non-steroidal anti-inflammatory drugs in the era of the COVID-19 pandemic in the context of the human and the environment. Sci. Total Environ. 2022, 834, 155317. [Google Scholar] [CrossRef] [PubMed]
- Copolovici, L.; Timis, D.; Taschina, M.; Copolovici, D.; Cioca, G.; Bungau, S. Diclofenac influence on photosynthethic parameters and volatile organic compounds emission from Phaseolus vulgaris L. plants. Rev. Chem. 2017, 68, 2076–2078. [Google Scholar]
- Ternes, T. Occurrence of drugs in German sewage treatment plants and rivers. Water Res. 1998, 32, 3245–3260. [Google Scholar] [CrossRef]
- Poddar, K.; Sarkar, D.; Chakraborty, D.; Patil, P.B.; Maity, S.; Sarkar, A. Paracetamol biodegradation by Pseudomonas strain PrS10 isolated from pharmaceutical effluents. Int. Biodeter. Biodegrad. 2022, 175, 105490. [Google Scholar] [CrossRef]
- Palma, T.L.; Magno, G.; Costa, M.C. Biodegradation of paracetamol by some gram-positive bacterial isolates. Curr. Microbiol. 2021, 78, 2774–2786. [Google Scholar] [CrossRef]
- Ivshina, I.B.; Tyumina, E.A.; Kuzmina, M.V.; Vikhareva, E.V. Features of diclofenac biodegradation by Rhodococcus ruber IEGM 346. Sci. Rep. 2019, 9, 9159. [Google Scholar] [CrossRef] [Green Version]
- Baranowska, I.; Kowalski, B. Using HPLC method with DAD detection for the simultaneous determination of 15 drugs in surface water and wastewater. Pol. J. Environ. Stud. 2011, 20, 21–28. [Google Scholar]
- Čelić, M.; Gros, M.; Farré, M.; Barceló, D.; Petrović, M. Pharmaceuticals as chemical markers of wastewater contamination in the vulnerable area of the Ebro Delta (Spain). Sci. Total Environ. 2019, 652, 952–963. [Google Scholar] [CrossRef]
- Shanmugam, G.; Sampath, S.; Selvaraj, K.K.; Larsson, D.G.J.; Ramaswamy, B.R. Non-steroidal anti-inflammatory drugs in Indian rivers. Environ. Sci. Pollut. Res. 2014, 21, 921–931. [Google Scholar] [CrossRef]
- González-Alonso, S.; Merino, L.M.; Esteban, S.; López de Alda, M.; Barceló, D.; Durán, J.J.; López-Martínez, J.; Aceña, J.; Pérez, S.; Mastroianni, N.; et al. Occurrence of pharmaceutical, recreational and psychotropic drug residues in surface water on the northern Antarctic Peninsula region. Environ. Pollut. 2017, 229, 241–254. [Google Scholar] [CrossRef]
- Wojcieszyńska, D.; Guzik, U. Naproxen in the environment: Its occurrence, toxicity to non-target organisms and biodegradation. Appl. Microbiol. Biotechnol. 2020, 104, 1849–1857. [Google Scholar] [CrossRef] [Green Version]
- Fu, Q.; Fedrizzi, D.; Kosfeld, V.; Schlechtriem, C.; Ganz, V.; Derrer, S.; Rentsch, D.; Hollender, J. Biotransformation changes bioaccumulation and toxicity of diclofenac in aquatic organisms. Environ. Sci. Technol. 2020, 54, 4400–4408. [Google Scholar] [CrossRef]
- Żur, J.; Piński, A.; Wojcieszyńska, D.; Smułek, W.; Guzik, U. Diclofenac degradation-enzymes, genetic background and cellular alterations triggered in diclofenac-metabolising strain Pseudomonas moorei KB4. Int. J. Mol. Sci. 2020, 21, 6786. [Google Scholar] [CrossRef]
- Marchlewicz, A.; Guzik, U.; Wojcieszyńska, D. Occurrence and biodegradation of ibuprofen in aquatic environment. Ochr. Sr. 2015, 37, 65–70. (In Polish) [Google Scholar]
- Marchlewicz, A.; Guzik, U.; Hupert-Kocurek, K.; Nowak, A.; Wilczyńska, S.; Wojcieszyńska, D. Toxicity and biodegradation of ibuprofen by Bacillus thuringiensis B1(2015b). Environ. Sci. Pollut. Res. 2017, 24, 7572–7584. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aulestia, M.; Flores, A.; Acosta-Jurado, S.; Santero, E.; Camacho, E.M. Genetic characterisation of the ibuprofen-degradative pathway of Rhizorhabdus wittichii MPO218. Appl. Environ. Microbiol. 2022, 88, e00388-22. [Google Scholar] [CrossRef] [PubMed]
- Moreira, I.S.; Bessa, V.S.; Murgolo, S.; Piccirillo, C.; Mascolo, G.; Castro, P.M.L. Biodegradation of diclofenac by the bacterial strain Labrys portucalensis F11. Ecotoxicol. Environ. Saf. 2018, 152, 104–113. [Google Scholar] [CrossRef] [PubMed]
- Sharma, K.; Kaushik, G.; Thotakura, N.; Raza, K.; Sharma, N.; Nimesh, S. Fate of ibuprofen under optimised batch biodegradation experiments using Micrococcus yunnanensis isolated from pharmaceutical sludge. Int. J. Environ. Sci. Technol. 2019, 16, 8315–8328. [Google Scholar] [CrossRef]
- Zhang, L.; Hu, J.; Zhu, R.; Zhou, Q.; Chen, J. Degradation of paracetamol by pure bacterial cultures and their microbial consortium. Appl. Microbiol. Biotechnol. 2013, 97, 3687–3698. [Google Scholar] [CrossRef]
- Ivshina, I.B.; Rychkova, M.I.; Vikhareva, E.V.; Chekryshkina, L.A.; Mishenina, I.I. Catalysis of the biodegradation of unusable medicines by alkanotrophic Rhodococci. Appl. Biochem. Microbiol. 2006, 42, 392–395. [Google Scholar] [CrossRef]
- Ivshina, I.B.; Tyumina, E.A.; Bazhutin, G.A.; Vikhareva, E.V. Response of Rhodococcus cerastii IEGM 1278 to toxic effects of ibuprofen. PLoS ONE 2021, 16, e0260032. [Google Scholar] [CrossRef] [PubMed]
- Chopra, S.; Kumar, D. Characteristic and growth kinetics of biomass of Citrobacter freundii strains PYI-2 and Citrobacter portucalensis YPI-2 during the biodegradation of ibuprofen. Int. Microbiol. 2022, 25, 615–628. [Google Scholar] [CrossRef]
- Chopra, S.; Kumar, D. Characterization and biodegradation of ibuprofen by Bacillus siamensis strain DSI-1 isolated from wastewater. Rend. Lincei. Sci. Fis. Nat. 2022, 33, 643–652. [Google Scholar] [CrossRef]
- Górny, D.; Guzik, U.; Hupert-Kocurek, K.; Wojcieszyńska, D. A new pathway for naproxen utilisation by Bacillus thuringiensis B1(2015b) and its decomposition in the presence of organic and inorganic contaminants. J. Environ. Manag. 2019, 239, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Marchlewicz, A.; Guzik, U.; Smułek, W.; Wojcieszyńska, D. Exploring the degradation of ibuprofen by Bacillus thuringiensis B1(2015b): The new pathway and factors affecting degradation. Molecules 2017, 22, 1676. [Google Scholar] [CrossRef] [PubMed]
- Żur, J.; Wojcieszyńska, D.; Hupert-Kocurek, K.; Marchlewicz, A.; Guzik, U. Paracetamol-toxicity and microbial utilisation. Pseudomonas moorei KB4 as a case study for exploring degradation pathway. Chemosphere 2018, 206, 192–202. [Google Scholar] [CrossRef] [PubMed]
- Żur, J.; Michalska, J.; Piński, A.; Mrozik, A.; Nowak, A. Effects of low concentration of selected analgesics and successive bioaugmentation of the activated sludge on its activity and metabolic diversity. Water 2020, 12, 1133. [Google Scholar] [CrossRef] [Green Version]
- Domaradzka, D.; Guzik, U.; Hupert-Kocurek, K.; Wojcieszyńska, D. Cometabolic degradation of naproxen by Planococcus sp. strain S5. Water Air Soil Pollut. 2015, 226, 297. [Google Scholar] [CrossRef] [Green Version]
- Marchlewicz, A.; Domaradzka, D.; Guzik, U.; Wojcieszyńska, D. Bacillus thuringiensis B1(2015b) is a gram-positive bacteria able to degrade naproxen and ibuprofen. Water Air Soil Pollut. 2016, 227, 197. [Google Scholar] [CrossRef] [Green Version]
- Greń, I.; Wojcieszyńska, D.; Guzik, U.; Perkosz, M.; Hupert-Kocurek, K. Enhanced biotransformation of mononitrophenols by Stenotrophomonas maltophilia KB2 in the presence of aromatic compounds of plant origin. World J. Microbiol. Biotechnol. 2010, 26, 289–295. [Google Scholar] [CrossRef]
- Guzik, U.; Greń, I.; Wojcieszyńska, D.; Łabużek, S. Isolation and characterisation of a novel strain of Stenotrophomonas maltophilia possessing various dioxygenases for monocyclic hydrocarbon degradation. Braz. J. Microbiol. 2009, 40, 285–291. [Google Scholar] [CrossRef]
- Wojcieszyńska, D.; Hupert-Kocurek, K.; Greń, I.; Guzik, U. High activity catechol 2,3-dioxygenase from the cresols—Degrading Stenotrophomonas maltophilia strain KB2. Int. Biodeter. Biodegr. 2011, 65, 853–858. [Google Scholar] [CrossRef]
- Wojcieszyńska, D.; Hupert-Kocurek, K.; Guzik, U. Factors affecting activity of catechol 2,3-dioxygenase from 2-chlorophenol-degrading Stenotrophomonas maltophilia strain KB2. Biocatal. Biotransform. 2013, 31, 141–147. [Google Scholar] [CrossRef]
- Asmar, A.T.; Collet, J.F. Lpp, The Braun lipoprotein, turns 50—Major achievements and remaining issues. FEMS Microbiol. Lett. 2018, 365, fny199. [Google Scholar] [CrossRef] [Green Version]
- Elhalag, K.M.; Messiha, N.A.S.; Emara, H.M.; Abdallah, S.A. Evaluation of antibacterial activity of Stenotrophomonas maltophilia against Ralstonia solanacearum under different application conditions. J. Appl. Microbiol. 2016, 120, 1629–1645. [Google Scholar] [CrossRef] [Green Version]
- Guzik, U.; Hupert-Kocurek, K.; Wojcieszyńska, D. Intradiol dioxygenases —The key enzymes in xenobiotics degradation. In Biodegradation of Hazardous and Special Products; Chamy, R., Rosenkranz, F., Eds.; InTech: Rijeka, Croatia, 2013; Chapter 7; pp. 129–153. ISBN 978-953-51-1155-9. [Google Scholar]
- She, Z.; Gao, M.; Jin, C.; Chen, Y.; Yu, J. Toxicity and biodegradation of 2,4-dinitrophenol and 3-nitrophenol in anaerobic systems. Process Biochem. 2005, 40, 3017–3024. [Google Scholar] [CrossRef]
- Xu, J.; Wang, B.; Zhang, W.-H.; Zhang, F.-J.; Deng, Y.-D.; Wang, Y.; Gao, J.-J.; Tian, Y.-S.; Peng, R.-H.; Yao, Q.-H. Biodegradation of p-nitrophenol by engineered strain. MB Express 2021, 11, 124. [Google Scholar] [CrossRef]
- Arora, P.K.; Sharma, A.; Mehta, R.; Shenoy, B.D.; Srivastava, A.; Singh, V.P. Metabolism of 4-chloro-2-nitrophenol in a Gram-positive bacterium, Exiguobacterium sp. PMA. Microb. Cell Fact. 2012, 11, 150. [Google Scholar] [CrossRef] [Green Version]
- Guzik, U.; Hupert-Kocurek, K.; Marchlewicz, A.; Wojcieszyńska, D. Enhancement of biodegradation potential of catechol 1,2-diooxygenase through its immobilisation in calcium alginate gel. Electron. J. Biotechnol. 2014, 17, 83–88. [Google Scholar] [CrossRef] [Green Version]
- Koh, E.-I.; Henderson, J.P. Microbial copper-binding siderophores at the host pathogen interface. J. Biol. Chem. 2015, 190, 18967. [Google Scholar] [CrossRef] [Green Version]
- Bertini, I.; Briganti, F.; Scozzafava, A. Aliphatic and aromatic inhibitors binding to the active site of catechol 2,3-dioxygenase from Pseudomonas putida mt-2. FEBS Lett. 1994, 343, 56–60. [Google Scholar] [CrossRef] [Green Version]
- Michalska, J.; Greń, I.; Żur, J.; Wasilkowski, D.; Mrozik, A. Impact of the biological cotreatment of the Kalina pond leachate on laboratory sequencing batch reactor operation and activated sludge quality. Water 2019, 11, 1539. [Google Scholar] [CrossRef] [Green Version]
- Sambrook, J.; Russell, D.W. Molecular Cloning: A Laboratory Manual, 3rd ed.; CSHLP, Cold Spring Harbor: New York, NY, USA, 2001. [Google Scholar]
- Bloemberg, G.V.; Wijfjes, A.H.M.; Lamers, G.E.M.; Stuurman, N.; Lugtenberg, B.J.J. Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere: New perspectives for studying microbial communities. Mol. Plant-Microbe Interact. 2000, 13, 1170–1176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mahillon, J.; Lereclus, D. Electroporation of Bacillus thuringiensis and Bacillus cereus. In Electrotransformation of Bacteria; Eynard, N., Teissie, J., Eds.; Springer: Berlin/Heidelberg, Germany, 2000; pp. 242–250. [Google Scholar]
- Płociniczak, T.; Sinkkonen, A.; Romantschuk, M.; Piotrowska-Seget, Z. Characterization of Enterobacter intermedius MH8b and its use for the enhancement of heavy metals uptake by Sinapis alba L. Appl. Soil Ecol. 2013, 63, 1–7. [Google Scholar] [CrossRef]
- Kosjek, T.; Heath, E.; Kompare, B. Removal of pharmaceutical residues in a pilot wastewater treatment plant. Anal. Bioanal. Chem. 2007, 387, 1379–1387. [Google Scholar] [CrossRef] [PubMed]
- Jeong, H.; Park, J.; Kim, H. Determination of NH4+ in environmental water with interfering substances using the modified Nessler method. J. Chem. 2013, 2013, 359217. [Google Scholar] [CrossRef] [Green Version]
- Sen, N.P.; Donaldson, B. Improved colorimetric method for determining nitrate and nitrate in foods. J. Assoc. Anal. Chem. 1978, 61, 1389–1394. Available online: https://pubmed.ncbi.nlm.nih.gov/730645 (accessed on 25 January 2023). [CrossRef]
- Petriconi, G.L.; Papee, H.M. On routine colorimetric determination of trace nitrates, by brucine, in the presence of chloride. Water Air Soil Pollut. 1971, 1, 42–49. [Google Scholar] [CrossRef]
- Wojcieszyńska, D.; Domaradzka, D.; Hupert-Kocurek, K.; Guzik, U. Bacterial degradation of naproxen—Undisclosed pollutant in the environment. J. Environ. Manag. 2014, 145, 157–161. [Google Scholar] [CrossRef]
System | Proportion of B1(2015b):KB4:KB2:S5 | Paracetamol 10 mg/L | Ibuprofen 5 mg/L | Naproxen 1 mg/L | Diclofenac 1 mg/L |
---|---|---|---|---|---|
S1 | 1:1:1:1 | 100 ± 0.00 | 100 ± 0.00 | 16.30 ± 5.10 | 16.25 ± 3.39 |
S2 | 2:2:1:1 | 100 ± 0.00 | 100 ± 0.00 | 43.15 ± 4.29 | 2.05 ± 9.40 |
S3 | 1:1:0:0 | 100 ± 0.00 | 100 ± 0.00 | 50.90 ± 2.67 | 32.68 ± 0.25 |
S4 | 1:1:1:0 | 100 ± 0.00 | 100 ± 0.00 | 53.32 ± 0.89 | 10.75 ± 1.33 |
S5 | 1:1:0:1 | 100 ± 0.00 | 100 ± 0.00 | 49.26 ± 4.53 | 17.55 ± 3.32 |
S6 | 2:1:0:0 | 100 ± 0.00 | 100 ± 0.00 | 41.64 ± 3.04 | 40.76 ± 3.04 |
S7 | 1:2:0:0 | 100 ± 0.00 | 100 ± 0.00 | 74.02 ± 1.83 | 28.99 ± 4.25 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Marchlewicz, A.; Guzik, U.; Hupert-Kocurek, K.; Wojcieszyńska, D. Evaluation of the Defined Bacterial Consortium Efficacy in the Biodegradation of NSAIDs. Molecules 2023, 28, 2185. https://doi.org/10.3390/molecules28052185
Marchlewicz A, Guzik U, Hupert-Kocurek K, Wojcieszyńska D. Evaluation of the Defined Bacterial Consortium Efficacy in the Biodegradation of NSAIDs. Molecules. 2023; 28(5):2185. https://doi.org/10.3390/molecules28052185
Chicago/Turabian StyleMarchlewicz, Ariel, Urszula Guzik, Katarzyna Hupert-Kocurek, and Danuta Wojcieszyńska. 2023. "Evaluation of the Defined Bacterial Consortium Efficacy in the Biodegradation of NSAIDs" Molecules 28, no. 5: 2185. https://doi.org/10.3390/molecules28052185
APA StyleMarchlewicz, A., Guzik, U., Hupert-Kocurek, K., & Wojcieszyńska, D. (2023). Evaluation of the Defined Bacterial Consortium Efficacy in the Biodegradation of NSAIDs. Molecules, 28(5), 2185. https://doi.org/10.3390/molecules28052185