Toxicity of Moxifloxacin on the Growth, Photosynthesis, Antioxidant System, and Metabolism of Microcystis aeruginosa at Different Phosphorus Levels
Abstract
:1. Introduction
2. Materials and Methods
2.1. Microalgal Strain and Culture Condition
2.2. Antibiotic Treatment
2.3. Analytical Procedures
2.3.1. Determination of Algal Growth
2.3.2. Determination of Chlorophyll Fluorescence
2.3.3. Determination of Photosynthetic Pigments
2.3.4. Determination of Oxidative Stress Biomarkers
2.3.5. Metabolites Analysis Based on GC-MS
2.3.6. Statistical Analyses
3. Results and Discussion
3.1. Effects of MOX on Cellular Growth
3.2. Effects of MOX on Chlorophyll Fluorescence
3.3. Effects of MOX on Photosynthetic Pigments
3.4. Effects of MOX on Oxidative Stress
3.5. Metabolic Response of M. aeruginosa to MOX
3.6. Perturbed Pathway of M. aeruginosa by MOX
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Valitalo, P.; Kruglova, A.; Mikola, A.; Vahala, R. Toxicological impacts of antibiotics on aquatic micro-organisms: A mini-review. Int. J. Hyg. Environ. Health 2017, 220, 558–569. [Google Scholar] [CrossRef] [PubMed]
- Klein, E.Y.; Van Boeckel, T.P.; Martinez, E.M.; Pant, S.; Gandra, S.; Levin, S.A.; Goossens, H.; Laxminarayan, R. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc. Natl. Acad. Sci. USA 2018, 115, E3463–E3470. [Google Scholar] [CrossRef]
- Nandi, A.; Pecetta, S.; Bloom, D.E. Global antibiotic use during the COVID-19 pandemic: Analysis of pharmaceutical sales data from 71 countries, 2020–2022. EClinicalMedicine 2023, 57, 101848. [Google Scholar] [CrossRef]
- Jinjin, W.; Peiyong, G.; Shengxiang, Z. Response of the cyanobacterium Microcystis flos-aquae to levofloxacin. Environ. Sci. Pollut. Res. Int. 2014, 21, 3858–3865. [Google Scholar]
- Yang, C.W.; Song, G.; Lim, W. A review of the toxicity in fish exposed to antibiotics. Comp. Biochem. Phys. C 2020, 237. [Google Scholar] [CrossRef] [PubMed]
- Wan, L.; Wu, Y.; Zhang, Y.; Zhang, W. Toxicity, biodegradation of moxifloxacin and gatifloxacin on Chlamydomonas reinhardtii and their metabolic fate. Ecotoxicol. Environ. Saf. 2022, 240, 113711. [Google Scholar] [CrossRef]
- Li, M.; Wei, D.; Zhao, H.; Du, Y. Genotoxicity of quinolones: Substituents contribution and transformation products QSAR evaluation using 2D and 3D models. Chemosphere 2014, 95, 220–226. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization. WHO Drug Information 2019, vol. 33, 1. WHO Drug Inf. 2019, 33, 1–42. [Google Scholar]
- Jia, A.; Wan, Y.; Xiao, Y.; Hu, J. Occurrence and fate of quinolone and fluoroquinolone antibiotics in a municipal sewage treatment plant. Water Res. 2012, 46, 387–394. [Google Scholar] [CrossRef]
- Ashfaq, M.; Khan, K.N.; Rasool, S.; Mustafa, G.; Saif-Ur-Rehman, M.; Nazar, M.F.; Sun, Q.; Yu, C.P. Occurrence and ecological risk assessment of fluoroquinolone antibiotics in hospital waste of Lahore, Pakistan. Environ. Toxicol. Pharmacol. 2016, 42, 16–22. [Google Scholar] [CrossRef]
- Wan, L.; Wu, Y.; Zhang, B.; Yang, W.; Ding, H.; Zhang, W. Effects of moxifloxacin and gatifloxacin stress on growth, photosynthesis, antioxidant responses, and microcystin release in Microcystis aeruginosa. J. Hazard. Mater. 2021, 409, 124518. [Google Scholar] [CrossRef]
- Li, Z.; Gao, X.; Bao, J.; Li, S.; Wang, X.; Li, Z.; Zhu, L. Evaluation of growth and antioxidant responses of freshwater microalgae Chlorella sorokiniana and Scenedesmus dimorphus under exposure of moxifloxacin. Sci. Total Environ. 2023, 858, 159788. [Google Scholar] [CrossRef] [PubMed]
- Davis, T.W.; Berry, D.L.; Boyer, G.L.; Gobler, C.J. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 2009, 8, 715–725. [Google Scholar] [CrossRef]
- Bai, F.; Gao, G.; Li, T.; Liu, J.; Li, L.; Jia, Y.; Song, L. Integrated physiological and metabolomic analysis reveals new insights into toxicity pathways of paraquat to Microcystis aeruginosa. Aquat. Toxicol. 2023, 259, 106521. [Google Scholar] [CrossRef]
- Wu, H.; Zhang, W.; Huang, X.; Gu, P.; Li, Q.; Luo, X.; Zheng, Z. Phosphorus conditions change the cellular responses of Microcystis aeruginosa to perfluorooctanoic acid. Sci. Total Environ. 2023, 903, 166707. [Google Scholar] [CrossRef] [PubMed]
- Zhao, L.; Xu, K.; Juneau, P.; Huang, P.; Lian, Y.; Zheng, X.; Zhong, Q.; Zhang, W.; Xiao, F.; Wu, B.; et al. Light modulates the effect of antibiotic norfloxacin on photosynthetic processes of Microcystis aeruginosa. Aquat. Toxicol. 2021, 235, 105826. [Google Scholar] [CrossRef]
- Mao, Y.; Yu, Y.; Ma, Z.; Li, H.; Yu, W.; Cao, L.; He, Q. Azithromycin induces dual effects on microalgae: Roles of photosynthetic damage and oxidative stress. Ecotoxicol. Environ. Saf. 2021, 222, 112496. [Google Scholar] [CrossRef]
- Zhong, X.; Zhu, Y.; Wang, Y.; Zhao, Q.; Huang, H. Effects of three antibiotics on growth and antioxidant response of Chlorella pyrenoidosa and Anabaena cylindrica. Ecotoxicol. Environ. Saf. 2021, 211, 111954. [Google Scholar] [CrossRef]
- Young, E.B.; Tucker, R.C.; Pansch, L.A. Alkaline Phosphatase in Freshwater -Epiphyte Assemblages: Regulation in Response to Phosphorus Supply and Localization. J. Phycol. 2010, 46, 93–101. [Google Scholar] [CrossRef]
- Yang, M.; Wang, X. Interactions between Microcystis aeruginosa and coexisting bisphenol A at different phosphorus levels. Sci. Total Environ. 2019, 658, 439–448. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Chen, S.; Chen, X.; Zhang, J.; Gao, B. Interactions between Microcystis aeruginosa and coexisting amoxicillin contaminant at different phosphorus levels. J. Hazard. Mater. 2015, 297, 83–91. [Google Scholar] [CrossRef]
- Che, F.; Du, M.; Yan, C. Arsenate biotransformation by Microcystis aeruginosa under different nitrogen and phosphorus levels. J. Environ. Sci. 2018, 66, 41–49. [Google Scholar] [CrossRef]
- Touloupakis, E.; Tartari, G.; Zittelli, G.C.; Torzillo, G. Growth and photosynthetic performance of Chlamydopodium fusiforme cells cultivated in BG11 and Bristol media. J. Appl. Phycol. 2020, 32, 145–152. [Google Scholar] [CrossRef]
- Xiong, J.-Q.; Kurade, M.B.; Patil, D.V.; Jang, M.; Paeng, K.-J.; Jeon, B.-H. Biodegradation and metabolic fate of levofloxacin via a freshwater green alga, Scenedesmus obliquus in synthetic saline wastewater. Algal Res. 2017, 25, 54–61. [Google Scholar] [CrossRef]
- Guo, Q.; Wei, D.; Zhao, H.; Du, Y. Predicted no-effect concentrations determination and ecological risk assessment for benzophenone-type UV filters in aquatic environment. Environ. Pollut. 2020, 256, 113460. [Google Scholar] [CrossRef] [PubMed]
- Pancha, I.; Chokshi, K.; Maurya, R.; Trivedi, K.; Patidar, S.K.; Ghosh, A.; Mishra, S. Salinity induced oxidative stress enhanced biofuel production potential of microalgae Scenedesmus sp. CCNM 1077. Bioresour. Technol. 2015, 189, 341–348. [Google Scholar] [CrossRef]
- Xiong, J.Q.; Kurade, M.B.; Kim, J.R.; Roh, H.S.; Jeon, B.H. Ciprofloxacin toxicity and its co-metabolic removal by a freshwater microalga Chlamydomonas mexicana. J. Hazard. Mater. 2017, 323, 212–219. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Mao, F.; Kirumba, G.C.; Jiang, C.; Manefield, M.; He, Y. Changes in metabolites, antioxidant system, and gene expression in Microcystis aeruginosa under sodium chloride stress. Ecotoxicol. Environ. Saf. 2015, 122, 126–135. [Google Scholar] [CrossRef]
- Sabatini, S.E.; Juarez, A.B.; Eppis, M.R.; Bianchi, L.; Luquet, C.M.; Rios de Molina Mdel, C. Oxidative stress and antioxidant defenses in two green microalgae exposed to copper. Ecotoxicol. Environ. Saf. 2009, 72, 1200–1206. [Google Scholar] [CrossRef]
- Liang, W.; Yixiao, W.; Huijun, D.; Weihao, Z. Toxicity, Biodegradation, and Metabolic Fate of Organophosphorus Pesticide Trichlorfon on the Freshwater Algae Chlamydomonas reinhardtii. J. Agric. Food. Chem. 2020, 68, 1645–1653. [Google Scholar]
- Huang, M.; Keller, A.A.; Wang, X.; Tian, L.; Wu, B.; Ji, R.; Zhao, L. Low Concentrations of Silver Nanoparticles and Silver Ions Perturb the Antioxidant Defense System and Nitrogen Metabolism in N(2)-Fixing Cyanobacteria. Environ. Sci. Technol. 2020, 54, 15996–16005. [Google Scholar] [CrossRef]
- Zhang, H.; Lu, L.; Zhao, X.; Zhao, S.; Gu, X.; Du, W.; Wei, H.; Ji, R.; Zhao, L. Metabolomics Reveals the “Invisible” Responses of Spinach Plants Exposed to CeO2 Nanoparticles. Environ. Sci. Technol. 2019, 53, 6007–6017. [Google Scholar] [CrossRef]
- Lai, Z.; Tsugawa, H.; Wohlgemuth, G.; Mehta, S.; Mueller, M.; Zheng, Y.; Ogiwara, A.; Meissen, J.; Showalter, M.; Takeuchi, K.; et al. Identifying metabolites by integrating metabolome databases with mass spectrometry cheminformatics. Nat. Methods 2018, 15, 53–56. [Google Scholar] [CrossRef] [PubMed]
- de Wilt, A.; Butkovskyi, A.; Tuantet, K.; Leal, L.H.; Fernandes, T.V.; Langenhoff, A.; Zeeman, G. Micropollutant removal in an algal treatment system fed with source separated wastewater streams. J. Hazard. Mater. 2016, 304, 84–92. [Google Scholar] [CrossRef]
- Carstensen, A.; Herdean, A.; Schmidt, S.B.; Sharma, A.; Spetea, C.; Pribil, M.; Husted, S. The Impacts of Phosphorus Deficiency on the Photosynthetic Electron Transport Chain. Plant Physiol. 2018, 177, 271–284. [Google Scholar] [CrossRef]
- Qi, H.; Wang, J.; Wang, Z. A comparative study of the sensitivity of F v/F m to phosphorus limitation on four marine algae. J. Ocean Univ. China 2013, 12, 77–84. [Google Scholar] [CrossRef]
- Cetner, M.D.; Kalaji, H.M.; Borucki, W.; Kowalczyk, K. Special issue in honour of Prof. Reto J. Strasser—Phosphorus deficiency affects the I-step of chlorophyll a fluorescence induction curve of radish. Photosynthetica 2020, 58, 671–681. [Google Scholar] [CrossRef]
- Wu, Y.; Wan, L.; Zhang, W.; Ding, H.; Yang, W. Resistance of cyanobacteria Microcystis aeruginosa to erythromycin with multiple exposure. Chemosphere 2020, 249, 126147. [Google Scholar] [CrossRef] [PubMed]
- Roopnarain, A.; Gray, V.M.; Sym, S.D. Phosphorus limitation and starvation effects on cell growth and lipid accumulation in Isochrysis galbana U4 for biodiesel production. Bioresour. Technol. 2014, 156, 408–411. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Guan, Y.; Gao, Q.; Tam, N.F.; Zhu, W. Cellular responses, biodegradation and bioaccumulation of endocrine disrupting chemicals in marine diatom Navicula incerta. Chemosphere 2010, 80, 592–599. [Google Scholar] [CrossRef]
- Dahmen-Ben Moussa, I.; Chtourou, H.; Karray, F.; Sayadi, S.; Dhouib, A. Nitrogen or phosphorus repletion strategies for enhancing lipid or carotenoid production from Tetraselmis marina. Bioresour. Technol. 2017, 238, 325–332. [Google Scholar] [CrossRef]
- Singh, D.P.; Khattar, J.S.; Rajput, A.; Chaudhary, R.; Singh, R. High production of carotenoids by the green microalga Asterarcys quadricellulare PUMCC 5.1.1 under optimized culture conditions. PLoS ONE 2019, 14, e0221930. [Google Scholar] [CrossRef] [PubMed]
- Cupellini, L.; Calvani, D.; Jacquemin, D.; Mennucci, B. Charge transfer from the carotenoid can quench chlorophyll excitation in antenna complexes of plants. Nat. Commun. 2020, 11, 662. [Google Scholar] [CrossRef]
- Baxter, A.; Mittler, R.; Suzuki, N. ROS as key players in plant stress signalling. J. Exp. Bot. 2014, 65, 1229–1240. [Google Scholar] [CrossRef]
- Mittler, R.; Zandalinas, S.I.; Fichman, Y.; Van Breusegem, F. Reactive oxygen species signalling in plant stress responses. Nat. Rev. Mol. Cell Biol. 2022, 23, 663–679. [Google Scholar] [CrossRef]
- Guo, J.; Peng, J.; Lei, Y.; Kanerva, M.; Li, Q.; Song, J.; Guo, J.; Sun, H. Comparison of oxidative stress induced by clarithromycin in two freshwater microalgae Raphidocelis subcapitata and Chlorella vulgaris. Aquat. Toxicol. 2020, 219, 105376. [Google Scholar] [CrossRef]
- Yisa, A.G.; Chia, M.A.; Sha’aba, R.I.; Gauji, B.; Gadzama, I.M.K.; Oniye, S.J. The antibiotic ciprofloxacin alters the growth, biochemical composition, and antioxidant response of toxin-producing and non-toxin-producing strains of Microcystis. J. Appl. Phycol. 2021, 33, 2145–2155. [Google Scholar] [CrossRef]
- Zhang, H.; Du, W.; Peralta-Videa, J.R.; Gardea-Torresdey, J.L.; White, J.C.; Keller, A.; Guo, H.; Ji, R.; Zhao, L. Metabolomics Reveals How Cucumber (Cucumis sativus) Reprograms Metabolites To Cope with Silver Ions and Silver Nanoparticle-Induced Oxidative Stress. Environ. Sci. Technol. 2018, 52, 8016–8026. [Google Scholar] [CrossRef]
- Wu, X.; Liu, Y.; Yin, S.; Xiao, K.; Xiong, Q.; Bian, S.; Liang, S.; Hou, H.; Hu, J.; Yang, J. Metabolomics revealing the response of rice (Oryza sativa L.) exposed to polystyrene microplastics. Environ. Pollut. 2020, 266, 115159. [Google Scholar] [CrossRef]
- Kondo, Y.; Ishitsuka, Y.; Kadowaki, D.; Kuroda, M.; Tanaka, Y.; Nagatome, M.; Irikura, M.; Hirata, S.; Sato, K.; Maruyama, T.; et al. Phosphoenolpyruvic acid, an intermediary metabolite of glycolysis, as a potential cytoprotectant and anti-oxidant in HeLa cells. Biol. Pharm. Bull. 2012, 35, 606–611. [Google Scholar] [CrossRef] [PubMed]
- Ye, G.; Ding, D.; Gao, H.; Chi, Y.; Chen, J.; Wu, Z.; Lin, Y.; Dong, S. Comprehensive metabolic responses of HepG2 cells to fine particulate matter exposure: Insights from an untargeted metabolomics. Sci. Total Environ. 2019, 691, 874–884. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Zhang, Y.; Du, Y.; Chen, S.; Tang, H. Dynamic metabonomic responses of tobacco (Nicotiana tabacum) plants to salt stress. J. Proteome Res. 2011, 10, 1904–1914. [Google Scholar] [CrossRef] [PubMed]
- Bentley, L.E. Occurrence of malonic acid in plants. Nature 1952, 170, 847–848. [Google Scholar] [CrossRef] [PubMed]
- Fernandez, O.; Bethencourt, L.; Quero, A.; Sangwan, R.S.; Clement, C. Trehalose and plant stress responses: Friend or foe? Trends Plant Sci. 2010, 15, 409–417. [Google Scholar] [CrossRef] [PubMed]
- Han, M.; Zhang, C.; Suglo, P.; Sun, S.; Wang, M.; Su, T. L-Aspartate: An Essential Metabolite for Plant Growth and Stress Acclimation. Molecules 2021, 26, 1887. [Google Scholar] [CrossRef] [PubMed]
- Arruda, P.; Barreto, P. Lysine Catabolism Through the Saccharopine Pathway: Enzymes and Intermediates Involved in Plant Responses to Abiotic and Biotic Stress. Front. Plant Sci. 2020, 11, 587. [Google Scholar] [CrossRef] [PubMed]
- Muthuramalingam, P.; Krishnan, S.R.; Pandian, S.; Mareeswaran, N.; Aruni, W.; Pandian, S.K.; Ramesh, M. Global analysis of threonine metabolism genes unravel key players in rice to improve the abiotic stress tolerance. Sci. Rep. 2018, 8, 9270. [Google Scholar] [CrossRef] [PubMed]
- Huang, L.; Fang, Z.; Gao, J.; Wang, J.; Li, Y.; Sun, L.; Wang, Y.; Liao, J.; Gooneratne, R. Protective role of L-threonine against cadmium toxicity in Saccharomyces cerevisiae. J. Basic Microbiol. 2021, 61, 339–350. [Google Scholar] [CrossRef] [PubMed]
- Huang, L.B.; Peng, L.N.; Yan, X.H. Multi-omics responses of red algae to intertidal desiccation during low tides. Algal Res. 2021, 58, 102376. [Google Scholar] [CrossRef]
- Chu, H.Q.; Ren, L.; Yang, L.B.; Chen, J.B.; Zhou, X.F.; Zhang, Y.L. Metabolomics reveals a lipid accumulation mechanism involving carbon allocation in under norfloxacin stress. Renew. Energy 2020, 157, 585–592. [Google Scholar] [CrossRef]
- Li, M.; Shi, X.; Guo, C.; Lin, S. Phosphorus Deficiency Inhibits Cell Division but Not Growth in the Dinoflagellate Amphidinium carterae. Front. Microbiol. 2016, 7, 826. [Google Scholar] [CrossRef]
- Kujawinski, E.B.; Longnecker, K.; Alexander, H.; Dyhrman, S.T.; Fiore, C.L.; Haley, S.T.; Johnson, W.M. Phosphorus availability regulates intracellular nucleotides in marine eukaryotic phytoplankton. Limnol. Oceanogr. Lett. 2017, 2, 119–129. [Google Scholar] [CrossRef]
- Forsgren, A.; Bredberg, A.; Pardee, A.B.; Schlossman, S.F.; Tedder, T.F. Effects of ciprofloxacin on eucaryotic pyrimidine nucleotide biosynthesis and cell growth. Antimicrob. Agents Chemother. 1987, 31, 774–779. [Google Scholar] [CrossRef] [PubMed]
Concentration (mg/L) | Equation | r2 | EC50 (μg/L) | PNEC (ng/L) |
---|---|---|---|---|
0.2 | y a = 6.42x b − 1.55 | 0.99 | 8.03 | 8.03 |
1 | y = 6.61x − 1.85 | 0.99 | 7.84 | 7.84 |
5 | y = 6.90x + 2.32 | 0.98 | 6.91 | 6.91 |
P Concentration | Perturbed Pathways | Match Status | p | Impact | Involved Metabolites |
---|---|---|---|---|---|
0.2 mg/L | Cysteine and methionine metabolism | 4/41 | 0.0084 | 0.1236 | 5′-Methylthioadenosine, L-Serine, L-Homoserine, L-Aspartate, |
Glyoxylate and dicarboxylate metabolism | 7/37 | 0.0110 | 0.2154 | Isocitrate, D-Glycerate, (S)-Malate, meso-Tartaric acid, Glycine, Succinate, L-Serine | |
Lysine degradation | 4/22 | 0.0179 | 0.2444 | L-Lysine, Cadaverine, 2-Oxoglutarate, Succinate | |
Alanine, aspartate, and glutamate metabolism | 6/22 | 0.0210 | 0.2154 | L-Aspartate, L-Asparagine, L-Alanine, 2-Oxoglutarate, Fumarate, Succinate | |
1 mg/L | Starch and sucrose metabolism | 6/22 | 0.0124 | 0.5114 | D-Fructose, Sucrose, D-Glucose, alpha-Trehalose, Maltose, D-Fructose 6-phosphate |
Pyrimidine metabolism | 5/51 | 0.0120 | 0.2061 | Uracil, Uridine, Thymine, 3-Hydroxypropanoate, Uridine 5′-diphosphate | |
Arginine and proline metabolism | 2/29 | 0.0223 | 0.1742 | Putrescine, L-Ornithine | |
Arginine biosynthesis | 7/16 | 0.0234 | 0.4088 | N-Acetylornithine, N-Acetyl-L-glutamate, L-Aspartate, L-Citrulline, L-Ornithine, 2-Oxoglutarate, Fumarate | |
Lysine degradation | 4/22 | 0.0300 | 0.2444 | L-Lysine, Cadaverine, 2-Oxoglutarate, Succinate | |
Glycerolipid metabolism | 2/15 | 0.0362 | 0.2191 | Glycerol, D-Glycerate | |
Cysteine and methionine metabolism | 4/41 | 0.0393 | 0.1236 | 5′-Methylthioadenosine, L-Serine, L-Homoserine, L-Aspartate | |
Glycine, serine, and threonine metabolism | 6/33 | 0.0473 | 0.5114 | Glycine, L-Aspartate, L-Threonine, L-Serine, L-Homoserine, D-Glycerate |
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Wan, L.; Zhou, Y.; Huang, R.; Jiao, Y.; Gao, J. Toxicity of Moxifloxacin on the Growth, Photosynthesis, Antioxidant System, and Metabolism of Microcystis aeruginosa at Different Phosphorus Levels. Toxics 2024, 12, 611. https://doi.org/10.3390/toxics12080611
Wan L, Zhou Y, Huang R, Jiao Y, Gao J. Toxicity of Moxifloxacin on the Growth, Photosynthesis, Antioxidant System, and Metabolism of Microcystis aeruginosa at Different Phosphorus Levels. Toxics. 2024; 12(8):611. https://doi.org/10.3390/toxics12080611
Chicago/Turabian StyleWan, Liang, Yan Zhou, Rong Huang, Yiying Jiao, and Jian Gao. 2024. "Toxicity of Moxifloxacin on the Growth, Photosynthesis, Antioxidant System, and Metabolism of Microcystis aeruginosa at Different Phosphorus Levels" Toxics 12, no. 8: 611. https://doi.org/10.3390/toxics12080611