The xenobiotic doxycycline affects nitrogen transformations in soil and impacts earthworms and cultivated plants

References

• Igel-Egalon, A.; Cheviron, N.; Hedde, M.; Hernandez-Raquet, G.; Mougin, C. ISTA 14-Impact of Antibiotics from Pig Slurry on Soil Microbial Communities, Including the Basidiomycete Trametes versicolor. Environ. Toxicol. 2012, 27, 129–136. DOI: 10.1002/tox.20623.
   PubMed Web of Science ®Google Scholar
• Wang, H.; Che, B.; Duan, A.; Mao, J.; Dahlgren, R. A.; Zhang, M.; Zhang, H.; Zeng, A.; Wang, X. Toxicity Evaluation of β-Diketone Antibiotics on the Development of Embryo-Larval Zebrafish (Danio rerio): Effects of β-Diketone Antibiotics. Environ. Toxicol. 2014, 29, 1134–1146. DOI: 10.1002/tox.21843.
   PubMed Web of Science ®Google Scholar
• Parpounas, A.; Litskas, V.; Hapeshi, E.; Michael, C.; Fatta-Kassinos, D. Assessing the Presence of Enrofloxacin and Ciprofloxacin in Piggery Wastewater and Their Adsorption Behaviour onto Solid Materials, with a Newly Developed Chromatographic Method. Environ. Sci. Pollut. Res. 2017, 24, 23371–23381. DOI: 10.1007/s11356-017-9849-9.
   PubMed Web of Science ®Google Scholar
• Wallace, J. S.; Garner, E.; Pruden, A.; Aga, D. S. Occurrence and Transformation of Veterinary Antibiotics and Antibiotic Resistance Genes in Dairy Manure Treated by Advanced Anaerobic Digestion and Conventional Treatment Methods. Environ. Pollut. 2018, 236, 764–772. DOI: 10.1016/j.envpol.2018.02.024.
   PubMed Web of Science ®Google Scholar
• Rahman, M. M.; Shan, J.; Yang, P.; Shang, X.; Xia, Y.; Yan, X. Effects of Long-Term Pig Manure Application on Antibiotics, Abundance of Antibiotic Resistance Genes (ARGs), Anammox and Denitrification Rates in Paddy Soils. Environ. Pollut. 2018, 240, 368–377. DOI: 10.1016/j.envpol.2018.04.135.
   PubMed Web of Science ®Google Scholar
• Karcı, A.; Balcıoğlu, I. A. Investigation of the Tetracycline, Sulfonamide, and Fluoroquinolone Antimicrobial Compounds in Animal Manure and Agricultural Soils in Turkey. Sci. Total Environ. 2009, 407, 4652–4664. DOI: 10.1016/j.scitotenv.2009.04.047.
   PubMed Web of Science ®Google Scholar
• Xie, X.; Zhou, Q.; Bao, Q.; He, Z.; Bao, Y. Genotoxicity of Tetracycline as an Emerging Pollutant on Root Meristem Cells of Wheat (Triticum aestivum L.). Environ. Toxicol. 2011, 26, 417–423. DOI: 10.1002/tox.20567.
   PubMed Web of Science ®Google Scholar
• Du, L.; Liu, W. Occurrence, Fate, and Ecotoxicity of Antibiotics in Agro-Ecosystems. A Review. Agron. Sustain. Dev. 2012, 32, 309–327. DOI: 10.1007/s13593-011-0062-9.
   Web of Science ®Google Scholar
• Ho, Y. B.; Zakaria, M. P.; Latif, P. A.; Saari, N. Occurrence of Veterinary Antibiotics and Progesterone in Broiler Manure and Agricultural Soil in Malaysia. Sci. Total Environ. 2014, 488–489, 261–267. DOI: 10.1016/j.scitotenv.2014.04.109.
   PubMed Web of Science ®Google Scholar
• Lundström, S. V.; Östman, M.; Bengtsson-Palme, J.; Rutgersson, C.; Thoudal, M.; Sircar, T.; Blanck, H.; Eriksson, K. M.; Tysklind, M.; Flach, C.-F.; Larsson, D. G. J. Minimal Selective Concentrations of Tetracycline in Complex Aquatic Bacterial Biofilms. Sci. Total Environ. 2016, 553, 587–595. DOI: 10.1016/j.scitotenv.2016.02.103.
   PubMed Web of Science ®Google Scholar
• Liu, S.; Xu, W.; Liu, Y.; Tan, X.; Zeng, G.; Li, X.; Liang, J.; Zhou, Z.; Yan, Z.; Cai, X. Facile Synthesis of Cu(II) Impregnated Biochar with Enhanced Adsorption Activity for the Removal of Doxycycline Hydrochloride from Water. Sci. Total Environ. 2017, 592, 546–553.
   PubMed Web of Science ®Google Scholar
• Bourdat-Deschamps, M.; Ferhi, S.; Bernet, N.; Feder, F.; Crouzet, O.; Patureau, D.; Montenach, D.; Moussard, G. D.; Mercier, V.; Benoit, P.; Houot, S. Fate and Impacts of Pharmaceuticals and Personal Care Products after Repeated Applications of Organic Waste Products in Long-Term Field Experiments. Sci. Total Environ. 2017, 607–608, 271–280. DOI: 10.1016/j.scitotenv.2017.06.240.
   PubMed Web of Science ®Google Scholar
• Pan, M.; Chu, L. M. Transfer of Antibiotics from Wastewater or Animal Manure to Soil and Edible Crops. Environ. Pollut. 2017, 231, 829–836. DOI: 10.1016/j.envpol.2017.08.051.
   PubMed Web of Science ®Google Scholar
• Christou, A.; Michael, C.; Fatta-Kassinos, D.; Fotopoulos, V. Can the Pharmaceutically Active Compounds Released in Agroecosystems be Considered as Emerging Plant Stressors? Environ. Int. 2018, 114, 360–364. DOI: 10.1016/j.envint.2018.03.003.
   PubMed Web of Science ®Google Scholar
• Fernández, C.; Alonso, C.; Babı́n, M. M.; Pro, J.; Carbonell, G.; Tarazona, J. V. Ecotoxicological Assessment of Doxycycline in Aged Pig Manure Using Multispecies Soil Systems. Sci. Total Environ. 2004, 323, 63–69. DOI: 10.1016/j.scitotenv.2003.10.015.
   PubMed Web of Science ®Google Scholar
• Daghrir, R.; Drogui, P. Tetracycline Antibiotics in the Environment: A Review. Environ. Chem. Lett. 2013, 11, 209–227. DOI: 10.1007/s10311-013-0404-8.
   Web of Science ®Google Scholar
• Kim, H. Y.; Yu, S.; Jeong, T.; Kim, S. D. Relationship between Trans-Generational Effects of Tetracycline on Daphnia magna at the Physiological and Whole Organism Level. Environ. Pollut. 2014, 191, 111–118. DOI: 10.1016/j.envpol.2014.04.022.
   PubMed Web of Science ®Google Scholar
• Peng, S.; Wang, Y.; Zhou, B.; Lin, X. Long-Term Application of Fresh and Composted Manure Increase Tetracycline Resistance in the Arable Soil of Eastern China. Sci. Total Environ. 2015, 506–507, 279–286. DOI: 10.1016/j.scitotenv.2014.11.010.
   PubMed Web of Science ®Google Scholar
• Wang, Z.; Du, Y.; Yang, C.; Liu, X.; Zhang, J.; Li, E.; Zhang, Q.; Wang, X. Occurrence and Ecological Hazard Assessment of Selected Antibiotics in the Surface Waters in and around Lake Honghu. China. Sci. Total Environ. 2017, 609, 1423–1432. DOI: 10.1016/j.scitotenv.2017.08.009.
   PubMed Web of Science ®Google Scholar
• Chen, Q.; Guo, X.; Hua, G.; Li, G.; Feng, R.; Liu, X. Migration and Degradation of Swine Farm Tetracyclines at the River Catchment Scale: Can the Multi-Pond System Mitigate Pollution Risk to Receiving Rivers?. Environ. Pollut. 2017, 220, 1301–1310. DOI: 10.1016/j.envpol.2016.11.004.
   PubMed Web of Science ®Google Scholar
• Zhang, X.-X.; Zhang, T. Occurrence, Abundance, and Diversity of Tetracycline Resistance Genes in 15 Sewage Treatment Plants across China and Other Global Locations. Environ. Sci. Technol. 2011, 45, 2598–2604. DOI: 10.1021/es103672x.
   PubMed Web of Science ®Google Scholar
• Szatmári, I.; Barcza, T.; Körmöczy, P. S.; Laczay, P. Ecotoxicological Assessment of Doxycycline in Soil. J. Environ. Sci. Health B 2012, 47, 129–135. DOI: 10.1080/03601234.2012.624476.
   PubMed Web of Science ®Google Scholar
• Kramer, L.; Grandi, G.; Passeri, B.; Gianelli, P.; Genchi, M.; Dzimianski, M. T.; Supakorndej, P.; Mansour, A. M.; Supakorndej, N.; McCall, S. D.; McCall, J. W. Evaluation of Lung Pathology in Dirofilaria immitis-Experimentally Infected Dogs Treated with Doxycycline or a Combination of Doxycycline and Ivermectin Before Administration of Melarsomine Dihydrochloride. Vet. Parasitol. 2011, 176, 357–360. DOI: 10.1016/j.vetpar.2011.01.021.
   PubMed Web of Science ®Google Scholar
• Brihoum, M.; Amory, H.; Desmecht, D.; Cassart, D.; Deleuze, S.; Rollin, F. Descriptive Study of 32 Cases of Doxycycline-Overdosed Calves. J. Vet. Intern. Med. 2010, 24, 1203–1210. DOI: 10.1111/j.1939-1676.2010.0560.x.
   PubMed Web of Science ®Google Scholar
• Castro Robles, L. J.; Sahagún Prieto, A. M.; Diez Liébana, M. J.; Martínez, N. F.; Vega, M. S.; Vieitez, J. J. G. Pharmacokinetic Behavior of Doxycycline after Intramuscular Injection in Sheep. Am. J. Vet. Res. 2012, 73, 714–718. DOI: 10.2460/ajvr.73.5.714.
   PubMed Web of Science ®Google Scholar
• Peng, P.; Wang, Y.; Liu, L.; Zou, Y.; Liao, X.; Liang, J.; Wu, Y. The Excretion and Environmental Effects of Amoxicillin, Ciprofloxacin, and Doxycycline Residues in Layer Chicken Manure. Poult. Sci. 2016, 95, 1033–1041.
   PubMed Web of Science ®Google Scholar
• Zhou, L.-J.; Ying, G.-G.; Liu, S.; Zhang, R.-Q.; Lai, H.-J.; Chen, Z.-F.; Pan, C.-G. Excretion Masses and Environmental Occurrence of Antibiotics in Typical Swine and Dairy Cattle Farms in China. Sci. Total Environ. 2013, 444, 183–195. DOI: 10.1016/j.scitotenv.2012.11.087.
   PubMed Web of Science ®Google Scholar
• Naeimi, S.; Faghihian, H. Remediation of Pharmaceutical Contaminated Water by Use of Magnetic Functionalized Metal Organic Framework. Physicochemical Study of Doxycycline Adsorption: Physicochemical Study of DOC Adsorption. Water Environ. J. 2018, 32, 422–432. DOI: 10.1111/wej.12343.
   Web of Science ®Google Scholar
• Walters, E.; McClellan, K.; Halden, R. U. Occurrence and Loss over Three Years of 72 Pharmaceuticals and Personal Care Products from Biosolids–Soil Mixtures in Outdoor Mesocosms. Water Res. 2010, 44, 6011–6020. DOI: 10.1016/j.watres.2010.07.051.
   PubMed Web of Science ®Google Scholar
• Pansu, M.; Gautheyrou, J. (Eds.). Handbook of Soil Analysis - Mineralogical, Organic and Inorganic. Springer: Berlin Heidelberg, Germany, 2006.
   Google Scholar
• Litskas, V. D.; Karamanlis, X. N.; Prousali, S. P.; Koveos, D. S. Effects of the Antibiotic Amoxicillin on Key Species of the Terrestrial Environment. Bull. Environ. Contam. Toxicol. 2018, 100, 509–515. DOI: 10.1007/s00128-018-2302-z.
   PubMed Web of Science ®Google Scholar
• OECD. Test No. 216: Soil Microorganisms: Nitrogen Transformation Test. Organisation for Economic Co-operation and Development: Paris, 2000.
   Google Scholar
• Bouyoucos, G. J. Hydrometer Method Improved for Making Particle Size Analyses of Soils. Agron. J. 1962, 54, 464. DOI: 10.2134/agronj1962.00021962005400050028x.
   Web of Science ®Google Scholar
• Walkley, A.; Black, I. A. An Examination of the Degtjareff Method for Determining Soil Organic Matter, and a Proposed Modification of the Chromic Acid Titration Method. Soil Sci. 1934, 37, 29. DOI: 10.1097/00010694-193401000-00003.
   Web of Science ®Google Scholar
• Schuman, G. E.; Stanley, M. A.; Knudsen, D. Automated Total Nitrogen Analysis of Soil and Plant Samples. Soil Sci. Soc. Am. J. 1973, 37, 480. DOI: 10.2136/sssaj1973.03615995003700030045x.
   Web of Science ®Google Scholar
• Thien, S. J.; Myers, R. Determination of Bioavailable Phosphorus in Soil. Soil Sci. Soc. Am. J. 1992, 56, 814–818. DOI: 10.2136/sssaj1992.03615995005600030023x.
   Web of Science ®Google Scholar
• Allison, L. E.; Brown, J. W.; Hayward, H. E.; Richards, A.; Bernstein, L.; Fireman, M.; Pearson, G. A.; Bower, C. A.; Hatcher, J. T.; Reeve, R. C. Diagnosis and Improvement of Saline and Alkali Soils. United States Salinity Laboratory Staff: Washington, USA, 1954.
   Google Scholar
• Vance, E. D.; Brookes, P. C.; Jenkinson, D. S. An Extraction Method for Measuring Soil Microbial Biomass C. Soil Biol. Biochem. 1987, 19, 703–707. DOI: 10.1016/0038-0717(87)90052-6.
   Web of Science ®Google Scholar
• OECD. Test No. 222: Earthworm Reproduction Test (Eisenia Fetida/Eisenia Andrei). Organisation for Economic Co-operation and Development: Paris, 2004.
   Google Scholar
• OECD. Test No. 208: Terrestrial Plant Test: Seedling Emergence and Seedling Growth Test. Organisation for Economic Co-operation and Development: Paris, 2006.
   Google Scholar
• Pino, M. R.; Val, J.; Mainar, A. M.; Zuriaga, E.; Español, C.; Langa, E. Acute Toxicological Effects on the Earthworm Eisenia fetida of 18 Common Pharmaceuticals in Artificial Soil. Sci. Total Environ. 2015, 518–519, 225–237. DOI: 10.1016/j.scitotenv.2015.02.080.
   PubMed Web of Science ®Google Scholar
• Lin, D.; Zhou, Q.; Xu, Y.; Chen, C.; Li, Y. Physiological and Molecular Responses of the Earthworm (Eisenia fetida) to Soil Chlortetracycline Contamination. Environ. Pollut. 2012, 171, 46–51. DOI: 10.1016/j.envpol.2012.07.020.
   PubMed Web of Science ®Google Scholar
• Pan, M.; Chu, L. M. Phytotoxicity of Veterinary Antibiotics to Seed Germination and Root Elongation of Crops. Ecotoxicol. Environ. Saf. 2016, 126, 228–237. DOI: 10.1016/j.ecoenv.2015.12.027.
   PubMed Web of Science ®Google Scholar
• Bellino, A.; Lofrano, G.; Carotenuto, M.; Libralato, G.; Baldantoni, D. Antibiotic Effects on Seed Germination and Root Development of Tomato (Solanum lycopersicum L.). Ecotoxicol. Environ. Saf. 2018, 148, 135–141. DOI: 10.1016/j.ecoenv.2017.10.006.
   PubMed Web of Science ®Google Scholar
• Moullan, N.; Mouchiroud, L.; Wang, X.; Ryu, D.; Williams, E. G.; Mottis, A.; Jovaisaite, V.; Frochaux, M. V.; Quiros, P. M.; Deplancke, B.; et al. Tetracyclines Disturb Mitochondrial Function Across Eukaryotic Models: A Call for Caution in Biomedical Research. Cell Rep. 2015, 10, 1681–1691. DOI: 10.1016/j.celrep.2015.02.034.
   PubMed Web of Science ®Google Scholar
• Migliore, L.; Godeas, F.; De Filippis, S. P.; Mantovi, P.; Barchi, D.; Testa, C.; Rubattu, N.; Brambilla, G. Hormetic Effect(s) of Tetracyclines as Environmental Contaminant on Zea Mays. Environ. Pollut. 2010, 158, 129–134. DOI: 10.1016/j.envpol.2009.07.039.
   PubMed Web of Science ®Google Scholar