Cell Adaptations of Rhodococci to Pharmaceutical Pollutants
Abstract
Against the background of atense environmental situation, the risk of drug pollution in the natural environment is steadily increasing. Pharmaceuticals entering open ecosystems can cause toxic effects in wildlife from molecular to population levels. The aim of this research was to examine the impact of pharmaceutical pollutants on rhodococci, which are typical representatives of soil actinobacteria and active biodegraders of these compounds. The pharmaceutical products used in this research werediclofenac sodium and ibuprofen, which are non-steroidal anti-inflammatory drugs (NSAIDs) that are widely used and frequently found in the environment. The most common cell adaptations of rhodococci to the effects of NSAIDs were changes in zeta potential, catalase activity, morphometric parameters and degree of hydrophobicity; elevated contents of total cellular lipids; and the formation of cell conglomerates. The findings demonstrated the adaptation mechanisms of rhodococci and their increased resistance to the toxic effects of the pharmaceutical pollutants.
Keywords: pharmaceutical pollutants, NSAIDs, diclofenac, ibuprofen, cell responses, Rhodococcus
References
[1] aus der Beek T, Weber FA, Bergmann A et al. Pharmaceuticals in the environment – Global occurrences and perspectives. Environmental Toxicology and Chemistry. 2016;35(4):823–835.
[2] Mezzelani M, Gorbi S, Fattorini D et al. Long-term exposure of Mytilus galloprovincialis to diclofenac, ibuprofen and ketoprofen: Insights into bioavailability, biomarkers and transcriptomic changes. Chemosphere. 2018;198:238–248.
[3] Balbi T, Montagna M, Fabbri R et al. Diclofenac affects early embryo development in the marine bivalve Mytilus galloprovincialis. Science of the Total Environment. 2018;642:601–609.
[4] Gonzalez-Rey M, Bebianno MJ. Does non-steroidal anti-inflammatory (NSAID) ibuprofen induce antioxidant stress and endocrine disruption in mussel Mytilus galloprovincialis? Environmental Toxicology and Pharmacology. 2012;33(2):361–371.
[5] Cory WC, Welch AM, Ramirez JN, Rein LC. Naproxen and its phototransformation products: Persistence and ecotoxicity to toad tadpoles (Anaxyrus terrestris), individually and in mixtures. Environmental Toxicology and Chemistry. 2019;38(9):2008– 2019.
[6] Ågerstrand M, Arnold K, Balshine S, et al. Emerging investigator series: Use
of behavioural endpoints in the regulation of chemicals. Environmental Science: Processes and Impacts. 2020;22(1):49–65.
[7] Pierattini EC, Francini A, Huber C et al. Poplar and diclofenac pollution: A focus on physiology, oxidative stress and uptake in plant organs. Science of the Total Environment. 2018;636:944–952.
[8] Drzymala J, Kalka J. Ecotoxic interactions between pharmaceuticals in mixtures: Diclofenac and sulfamethoxazole. Chemosphere. 2020;259:1–12.
[9] Richmond EK, Rosi EJ, Walters DM et al. A diverse suite of pharmaceuticals contaminates stream and riparian food webs. Nature Communications. 2018;9(1):1–9.
[10] KüsterA, Adler N. Pharmaceuticals in the environment: Scientific evidence of risks and its regulation. Philosophical Transactions of the Royal Society B: Biological Sciences. 2014;369(1656):1–8.
[11] Palyzová A, Marešová H, Novák J, Zahradník J, Rezanka T. Effect of the antiinflammatory drug diclofenac on lipid composition of bacterial strain Raoultella sp. KDF8. Folia Microbiologica. 2020;65(4):763–773.
[12] Jiang C, Geng J, Hu H, Ma H, Gao X, Ren H. Impact of selected non-steroidal anti-inflammatory pharmaceuticals on microbial community assembly and activity in sequencing batch reactors. PLOS ONE.2017;12:1–16.
[13] Ding T, Yang M, Zhang J, et al. Toxicity, degradation and metabolic fate of ibuprofen on freshwater diatom Navicula sp. Journal of Hazardous Materials. 2017;330:127– 134.
[14] Alygizakis NA, Gago-Ferrero P, Borova VL, Pavlidou A, Hatzianestis I, Thomaidis NS. Occurrence and spatial distribution of 158 pharmaceuticals, drugs of abuse and related metabolites in offshore seawater. Science of the Total Environment. 2016;541:1097–1105.
[15] Rivera-Jaimes JA, Postigo C, Melgoza-Alemán RM, et al. Study of pharmaceuticals in surface and wastewater from Cuernavaca, Morelos, Mexico: Occurrence and environmental risk assessment. Science of the Total Environment. 2018;613:1263– 1274.
[16] Simazaki D, Kubota R, Suzuki T, Akiba M, Nishimura T, Kunikane SOccurrence of selected pharmaceuticals at drinking water purification plants in Japan and implications for human health. Water Research. 2015;76:187–200.
[17] Oaks, J & Gilbert, Martin & Virani, Munir et al. Diclofenac residues as the cause of vulture population decline in Pakistan. Nature. 2004;427(6975):630–633.
[18] Yokota H, Taguchi Y, Tanaka Y, et al. Chronic exposure to diclofenac induces delayed mandibular defects in medaka (Oryzias latipes) in a sex-dependent manner. Chemosphere. 2018; 210:139–146.
[19] Ivshina, Irina & Tyumina, Elena & Kuzmina, Maria & Vikhareva, Elena. Features of diclofenac biodegradation by Rhodococcus ruber IEGM 346. Scientific Reports. 2019;9(1):1–13.
[20] Bazhutin G, Shirinkina L, Tyumina E. Biodestruction of pharmapollutant ibuprofen (in Russian). Presented at: All-Russian Congress “Synbiosis-Russia 2019”, Perm, Russia; 2019. May 13-15
[21] Catalogue of strains of regional specialized collection of alkanotrophic microorganisms. Iegmcol.ru. 01/04/2018. Available from http://www.iegmcol.ru/strains/index.html.
[22] Neumann G, Veeranagouda Y, Karegoudar TB, et al. Cells of Pseudomonas putida and Enterobacter sp. adapt to toxic organic compounds by increasing their size. Extremophiles 2005;9(2)163–168. doi: 10.1007/s00792-005-0431-x.
[23] Gogoleva OA, Nemtseva NV, Bukharin OV. Catalase activity of hydrocarbon-oxidizing bacteria. Applied Biochemistry and Microbiology. 2012;48(6):552–556.
[24] Lindahl M, Faris A, Wadström T, Hjertén S. A new test based on “salting out” to measure relative hydrophobicity of bacterial cells. BBA – General Subjects. 1981;677(3–4):471–476.
[25] Mattos-Guaraldi AL, Formiga LCD, Andrade AFB. (1999). Cell surface hydrophobicity of sucrose fermenting and nonfermenting Corynebacterium diphtheriae strains evaluated by different methods. Current Microbiology. 1999;38(1):37–42.
[26] Di Gioia D, Fambrini L, Coppini E, Fava F, Barberio C. Aggregation-based cooperation during bacterial aerobic degradation of polyethoxylated nonylphenols. Research in Microbiology. 2004;155(9):761–769.
[27] Weathers TS, Higgins CP, Sharp JO.Enhanced biofilm production by a toluenedegrading Rhodococcus observed after exposure to perfluoroalkyl acids. Environmental Science and Technology. 2015;49(9):5458–5466. doi: 10.1021/es5060034.
[28] Veeranagouda Y, Karegoudar TB, Neumann G, Heipieper HJ.Enterobacter sp. VKGH12 growing with n-butanol as the sole carbon source and cells to which the alcohol is added as pure toxin show considerable differences in their adaptive responses. FEMS Microbiology Letters. 2006;254(1):48–54.
[29] Halder, Suman & Yadav, Kirendra & Sarkar, Ratul et al. Alteration of zeta potential and membrane permeability in bacteria: A study with cationic agents. SpringerPlus. 2015;4:1–14.