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Tetracycline uptake and metabolism by vetiver grass (Chrysopogon zizanioides L. Nash)

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Abstract

Environmental contamination by antibiotics not only perturbs the ecological balance but also poses a risk to human health by promoting the development of multiantibiotic-resistant bacteria. This study focuses on identifying the biochemical pathways associated with tetracycline (TC) transformation/degradation in vetiver grass that has the potential to be used as a biological remediation system in TC-contaminated water sources. A hydroponic experimental setup was used with four initial TC concentrations (0, 5, 35, 75 ppm), and TC uptake was monitored over a 30-day period. Results show that TC transformation in the media occurred during the first 5 days, where a decrease in the parent compound and an increase in the concentration of the isomers such as epitetracycline (ETC) and anhyrotetracycline (ATC) occurred, and TC disappeared in 20 days in tanks with vetiver grass. However, the isomers ETC and ATC remained in the control tanks for the duration of the trial. Transformation products of TC in plant tissue were analyzed by using ultra HPLC high-resolution Orbitrap mass spectrometery (HRMS/MS), which indicates amide hydrolysis of TC in vetiver roots. Metabolic profiling revealed that glyoxylate metabolism, TCA cycle, biosynthesis of secondary metabolites, tryptophan metabolism, and inositol phosphate metabolism were impacted in vetiver root by TC treatment.

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References

  • Alcázar R, Planas J, Saxena T, Zarza X, Bortolotti C, Cuevas J, Bitrián M, Tiburcio A, Altabella T (2010) Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants over-expressing the homologous arginine decarboxylase 2 gene. Plant Physiol Biochem 48:547–522

    Article  Google Scholar 

  • Aslund MLW, McShane H, Simpson AJ, Whalen JK, Hendershot WH, Sunhara GI (2012) Earthworm sublethal responses to titanium dioxide nanomaterial in soil detected by 1 H NMR metabolomics. Environ Sci Technol 46:1111–1118

    Article  Google Scholar 

  • Baltrėnaitė E, Lietuvninkas A, Baltrėnas P (2012) Use of dynamic factors to assess metal uptake and transfer in plants—example of trees. Water Air Soil Pollut 223:4297–4306

    Article  Google Scholar 

  • Bitrián M, Zarza X, Altabella T, Iburcio AF, Alcázar R (2012) Polyamines under abiotic stress: metabolic crossroads and hormonal crosstalks in plants. Metabolites 2:516–528

    Article  Google Scholar 

  • Carvalho PN, Basto MCP, Almeida CMR (2012) Potential of Phragmites australis for the removal of veterinary pharmaceuticals from aquatic media. Bioresour Technol 116:497–501

    Article  CAS  Google Scholar 

  • Chen Y, Shen Z, Li X (2004) The use of vetiver grass (Vetiveria zizanioides) in the phytoremediation of soils contaminated with heavy metals. Appl Geochem 19:1553–1565

    Article  CAS  Google Scholar 

  • Datta R, Das P, Smith S, Punamiya P, Ramanathan DM, Reddy R, Sarkar D (2013) Phytoremdiation potential of tetracycline by vetiver grass Chrysopogon zizanioides (L.) for tetracycline. Int J Phytorem 15:343–351

    Article  CAS  Google Scholar 

  • De Cazes M, Belleville M-P, Petit E, Llorca M, Rodriguez-Mozaz S, de Gunzburg J, Barcelo D, Sanchez-Marcano J (2014) Design and optimization of an enzymatic membrane reactor for tetracycline membrane. Catal Today 236:146–152

    Article  CAS  Google Scholar 

  • Denance N, Vallet AS, Goffner D, Molina A (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4:155

    Article  Google Scholar 

  • Di Marco G, Gismondi A, Canuti L, Scimeca M, Volpe A, Canini A (2014) Tetracycline accumulates in Iberis sempervirens L. Through apoplastic transport inducing oxidative stress and growth inhibition. Plant Biol 16(4):792–800

    Article  CAS  Google Scholar 

  • Dolliver H, Kumar K, Gupta S (2007) Sulfamethazine uptake by plants from manure-amended soil. J Environ Qual 36:1224–1230

    Article  CAS  Google Scholar 

  • Doskey, CM (2012) Phytoremediation of hexahydro-1,3,5-trinitro-1,3,5-triazine by Chrysopogon zizanioides. M.S. thesis. Michigan Technological University, Houghton, MI.

  • Dubey S, Misra P, Dwivedi S, Chatterjee S, Bag SK, Mantri S, Asif MH, Rai A, Kumar S, Shri M, Tripathi P, Tripathi RD, Trivedi PK, Chakrabarty D, Tμi RK (2010) Transcriptomic and metabolomic shifts in rice roots in response to Cr (VI) stress. BMC Genomics 11:648–666

    Article  Google Scholar 

  • Farkas MH, Berry OM, Aga DS (2007) Chlorotetracycline detoxification in maize via induction of glutathione S-transferases after antibiotic exposure. Environ Sci Technol 41:1450–1456

    Article  CAS  Google Scholar 

  • Fatta-Kassinos D, Meric S, Nikolaou A (2011) Pharmaceutical residues in environmental waters and wastewater: current state of knowledge and future research. Anal Bioanal Chem 399:251–275

    Article  CAS  Google Scholar 

  • Finley RL, Collignon P, Larsson DGJ, McEwen SA, Li X-Z, Gaze WH, Reid-Smith R, Timinouni M, Graham DW, Topp E (2013) The scourge of antibiotic resistance: the important role of the environment. Clin Infect Dis 57(5):704–710

    Article  Google Scholar 

  • Gujrathi NP, Haney B, Linden J (2005) Phytoremediation potential of M. aquaticum and P. stratiotes to modify antibiotic growth promoters, tetracycline, and oxytetracycline in aqueous wastewater systems. Int J Phytorem 7:99–112

    Article  Google Scholar 

  • Halling-Sørensen B, Sengelov G, Tjornelund J (2002) Toxicity of tetracycline degradation products to environmentally relevant bacteria, including selected tetracycline resistant bacteria. Arch Environ Cont Tox 42:263–271

    Article  Google Scholar 

  • Hong ZL, Lakkineni K, Zhang ZM (2000) Removal of feedback inhibition of DELTA 1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136

    Article  CAS  Google Scholar 

  • Hu X, Zhou Q (2014) Novel hydrated ribbon unexpectedly promotes aged seed germination and root differentiation. Scientific Reports 4:3782. doi:10.1038/srep03782

    Google Scholar 

  • Hu X, Zhou Q, Luo Y (2010) Occurrence and source analysis of typical veterinary antibiotics in manure, soil, vegetables and ground water from organic vegetable bases, northern China. Environ Pollut 158:2992–2998

    Article  CAS  Google Scholar 

  • Jia A, Xiaoa Y, Hua J, Asamib M, Kunikane S (2009) Simultaneous determination of tetracycline and their degradation products in environmental waters by liquid chromatography-electrospray tandem mass spectrometry. J Chromatogr A 1216:4655–4662

    Article  CAS  Google Scholar 

  • Kummerer K (2009a) Antibiotics in the aquatic environment-a review-part I. Chemosphere 75:417–434

    Article  Google Scholar 

  • Kummerer K (2009b) The presence of pharmaceuticals in the environment due to human use-present knowledge and future challenges. J Environ Manag 90:2354–2366

    Article  Google Scholar 

  • Li K, Pidatala VR, Shaik R, Datta R, Wusirika R (2014) Integrated metabolic and proteomic approaches dissect the effect of metal resistant bacteria on maize biomass and copper uptake. Environ Sci Technol 48(2):1184–1193

    Article  CAS  Google Scholar 

  • Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protocols 1:387–396

    Article  CAS  Google Scholar 

  • Lopez-Perez L, del Carmen M-BM, Maurel C, Carvajal M (2009) Changes in plasma membrane lipids, aquaporins and proton pump of broccoli roots, as an adaptation mechanism to salinity. Phytochem 70(4):492–500

    Article  CAS  Google Scholar 

  • Lytovchenko A, Beleggia R, Schauer N, Isaacson T, Leuendorf JE, Hellmann H, Rose JKC, Fernie AR (2009) Application of GC-MS for the detection of lipophilic compounds in diverse plant tissues. Plant Meth 5:4

    Article  Google Scholar 

  • Makhijani M, Gahlawat S, Chauhan K, Valsangkar S, Gauba P (2014) Phytoremediation potential of Cicer arietinum for tetracycline. Int J genet Eng. Biotechnol 5(2):153–160

    Google Scholar 

  • McCutcheon SC, Schnoor JL (2003) Phytoremediation: transformation and control of contaminants. Wiley, New York

    Book  Google Scholar 

  • Mortimer M, Kasemets K, Vodovnik M, Marinsek-Logar R, Kahru A (2011) Exposure to CuO nanoparticles changes the fatty acid composition of protozoa Tetrahymena thermophile. Environ Sci Technol 45:6617–6624

    Article  CAS  Google Scholar 

  • Pena A, Carmona A, Barbosa A, Lino C, Silveira I, Castillo B (1998) Determination of tetracycline and its major degradation products by liquid chromatography with fluorescence detection. J Pharmaceut Biomed 18:839–845

    Article  CAS  Google Scholar 

  • Price J, Laxmi A, St. Martin SK, Janga J-C (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16(8):2128–2150

    Article  CAS  Google Scholar 

  • Rehman MSU, Rashid N, Ashfaq M, Saif A, Ahmad N, Han JL (2015) Global risk of pharmaceutical contamination from highly populated developing countries. Chemosphere 138:1045–1055

    Article  CAS  Google Scholar 

  • Rizzo L, Manaia CM, Merlin C, Schwartz T, Dagot C, Ploy MC, Michael I, Fatta-Kassinos D (2013) Urban wastewater treatment plants as hotspots for antibiotic resistance spreading into the environment. Sci Total Environ 447:345–360

  • Sall J, Creighton L, Lehman A (2005) JMP Start Statistics, Fourth Ed. SAS Institute, Cary, NC and Pacific Grove, CA

  • Sarmah AK, Meyer MT, Boxall ABA (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (Vas) in the environment. Chemosphere 65:725–759

    Article  CAS  Google Scholar 

  • Schröder P, Collins CJ (2002) Conjugating enzymes involved in xenobiotic metabolism of organic xenobiotics in plants. Int J Phytorem 4:247–265

    Article  Google Scholar 

  • Sokol J, Matisova E (1994) Determination of tetracycline antibiotics in animal tissues of food-producing animals by high-performance liquid chromatography using solid-phase extraction. J Chromatogr A 669(1–2):75–80

    Article  CAS  Google Scholar 

  • Strong P-J, Claus H (2011) Laccase: a review of its past and its future in bioremediation. Crit Review Environ Sci Technol 41:373–434

    Article  Google Scholar 

  • Truong P, Foong YK, Guthrie M, Hung Y-T (2010) Phytoremediation of heavy metal contaminated soils and water using vetiver grass. In: Wang LK, Tay J-W, Tay STL, Hung Y-T (eds) Environmental bioengineering, handbook of environmental engineering, vol 10. Humana Press, New York, pp. 233–275

    Chapter  Google Scholar 

  • Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond Ser B Biol Sci 355:1517–1529

    Article  CAS  Google Scholar 

  • Xia J, Mandal R, Sinelnikov I, Broadhurst D, Wishart DS (2012) MetaboAnalyst 2.0—a comprehensive server for metabolomics data analysis. Nucl Acids Res 40:W127–W137

    Article  CAS  Google Scholar 

  • Xie X, Zhou Q, Lin D, Guo J, Bao Y (2011) Toxic effect of tetracycline exposure on growth, antioxidative and genetic indices of wheat (Triticum aestivum L.). Environ Sci Pollut Res 18:566–557

    Article  CAS  Google Scholar 

  • Yang L, Tang R, Zhi J, Liu H, Mueller-Roeber B, Xia H, Zhang H (2008) Enhancement of stress tolerance in transgenic tobacco plants constitutively expressing AtIpk2β, an inositol polyphosphate 6-/3-kinase from Arabidopsis thaliana. Plant Mol Biol 66(4):329–343

    Article  CAS  Google Scholar 

  • Ye Y, Zhang L, Hao F, Zhang J, Wang Y, Yang H (2012) Global metabolomic responses of Escherichia coli to heat stress. J Proteome Res 11:2559–2566

    Article  CAS  Google Scholar 

  • Zhang ZB, Yang G, Arana F, Chen Z, Li Y, Xia HJ (2007) Arabidopsis inositol polyphosphate 6-/3-kinase (Atlpk2b) is involved in axillary shoot branching via auxin signaling. Plant Physiol 144:942–951

    Article  CAS  Google Scholar 

  • Zheng R, Chen Z, Cai C, Tie B, Liu X, Reid BJ, Huang Q, Lei M, Sun G, Baltrėnaitė E (2015) Mitigating heavy metal accumulation into rice (Oryza sativa L.) using biochar amendment--a field experiment in Hunan, China. Environ. Sci. Pollut. Res. Int. 22(14):11097–11108

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Acknowledgments

The authors would like to thank Kate Waring for help in collection of data and establishing method for the solid-phase extraction experiment. AS gratefully acknowledges graduate assistantship from the Biological Sciences Department, Michigan Tech.

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Authors and Affiliations

  1. Department of Biological Sciences, Michigan Technological University, Houghton, MI, USA

    Aparupa Sengupta, Susan Bagley & Rupali Datta

  2. Department of Civil, Environmental and Ocean Engineering, Stevens Institute of Technology, Hoboken, NJ, USA

    Dibyendu Sarkar & Saumik Panja

  3. Department of Biology, Nazareth College, Rochester, NY, USA

    Padmini Das

  4. New Jersey Center for Science, Technology and Mathematics, Kean University, Union, NJ, USA

    Chinmayi Parikh & Dilrukshi Ramanathan

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  1. Aparupa Sengupta
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  2. Dibyendu Sarkar
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Correspondence to Rupali Datta.

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Responsible editor: Yi-ping Chen

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Sengupta, A., Sarkar, D., Das, P. et al. Tetracycline uptake and metabolism by vetiver grass (Chrysopogon zizanioides L. Nash). Environ Sci Pollut Res 23, 24880–24889 (2016). https://doi.org/10.1007/s11356-016-7688-8

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  • DOI: https://doi.org/10.1007/s11356-016-7688-8

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