Abstract
Although a variety of whole-cell biosensors and biosorbents have been developed for detection and removal of heavy metal contaminants, few whole cells can be applied to both monitoring and remediation of copper pollution in water. In this study, a modified plasmid was constructed by incorporating a copper-sensing element and a copper-adsorbing element into a temperature-inducible plasmid, pBV220. This plasmid was subsequently transformed into an engineered Escherichia coli strain lacking copA and cueO. This dual-functional E. coli cell selectively responded to copper ions with a linear detection range of 0.01–25 μM at 37 °C and could express surface-displayed CueR when treated at 42 °C without any costly chemical inducers. The display of CueR on the cell surface specifically enhanced its copper adsorption capacity and rapidly removed copper ions from aqueous solutions. In addition, the CueR surface-displayed cells could be regenerated by adsorption-desorption cycles via pH regulation. Moreover, by simply using two different temperatures, the detection or adsorption of copper using this dual-functional whole cell was achieved without any cross-interference. Most importantly, it provided highly sensitive, accurate quantification, and effective removal of copper in real environmental water samples. Thus, this E. coli cell can be used for large-scale detection and remediation of copper pollutants.
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References
Bilal M, Shah JA, Ashfaq T, Gardazi SM, Tahir AA, Pervez A, Haroon H, Mahmood Q (2013) Waste biomass adsorbents for copper removal from industrial wastewater--a review. J Hazard Mater 263(Pt 2):322–333. https://doi.org/10.1016/j.jhazmat.2013.07.071
Blake D, Nar M, D'Souza NA, Glenn JB, Klaine SJ, Roberts AP (2014) Treatment with coated layer double hydroxide clays decreases the toxicity of copper-contaminated water. Arch Environ Contam Toxicol 66(4):549–556. https://doi.org/10.1007/s00244-013-9986-1
Changela A, Chen K, Xue Y, Holschen J, Outten CE, O’Halloran TV, Mondragon A (2003) Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science (New York, NY) 301(5638):1383–1387. https://doi.org/10.1126/science.1085950
Cox DW, Moore SD (2002) Copper transporting P-type ATPases and human disease. J Bioenerg Biomembr 34(5):333–338
Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97(12):6640–6645. https://doi.org/10.1073/pnas.120163297
Fu F, Wang Q (2011) Removal of heavy metal ions from wastewaters: a review. J Environ Manag 92(3):407–418. https://doi.org/10.1016/j.jenvman.2010.11.011
Grass G, Rensing C (2001) Genes involved in copper homeostasis in Escherichia coli. J Bacteriol 183(6):2145–2147. https://doi.org/10.1128/jb.183.6.2145-2147.2001
Hakkila KM, Nikander PA, Junttila SM, Lamminmaki UJ, Virta MP (2011) Cd-specific mutants of mercury-sensing regulatory protein MerR, generated by directed evolution. Appl Environ Microbiol 77(17):6215–6224. https://doi.org/10.1128/aem.00662-11
Hu B, Li J, Yu W, Fang J (1993) Cloning of human prourokinase cDNA without the signal peptide and expression in Escherichia coli. Chin J Biotechnol 9(2):95–101
Hynninen A, Tonismann K, Virta M (2010) Improving the sensitivity of bacterial bioreporters for heavy metals. Bioeng Bugs 1(2):132–138. https://doi.org/10.4161/bbug.1.2.10902
Kanellis VG (2018) Sensitivity limits of biosensors used for the detection of metals in drinking water. Biophys Rev 10(5):1415–1426. https://doi.org/10.1007/s12551-018-0457-9
Kang Y, Lee W, Kim S, Jang G, Kim BG, Yoon Y (2018) Enhancing the copper-sensing capability of Escherichia coli-based whole-cell bioreporters by genetic engineering. Appl Microbiol Biotechnol 102(3):1513–1521. https://doi.org/10.1007/s00253-017-8677-7
Li PS, Peng ZW, Su J, Tao HC (2014) Construction and optimization of a Pseudomonas putida whole-cell bioreporter for detection of bioavailable copper. Biotechnol Lett 36(4):761–766. https://doi.org/10.1007/s10529-013-1420-2
Messerschmidt K, Hochrein L, Dehm D, Schulz K, Mueller-Roeber B (2016) Characterizing seamless ligation cloning extract for synthetic biological applications. Anal Biochem 509:24–32. https://doi.org/10.1016/j.ab.2016.05.029
Outten FW, Outten CE, Hale J, O’Halloran TV (2000) Transcriptional activation of an Escherichia coli copper efflux regulon by the chromosomal MerR homologue, cueR. J Biol Chem 275(40):31024–31029. https://doi.org/10.1074/jbc.M006508200
Rapisarda VA, Montelongo LR, Farias RN, Massa EM (1999) Characterization of an NADH-linked cupric reductase activity from the Escherichia coli respiratory chain. Arch Biochem Biophys 370(2):143–150. https://doi.org/10.1006/abbi.1999.1398
Ravikumar S, Yoo IK, Lee SY, Hong SH (2011) Construction of copper removing bacteria through the integration of two-component system and cell surface display. Appl Biochem Biotechnol 165(7-8):1674–1681. https://doi.org/10.1007/s12010-011-9386-9
Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27(2-3):197–213. https://doi.org/10.1016/s0168-6445(03)00049-4
Rensing C, Fan B, Sharma R, Mitra B, Rosen BP (2000) CopA: An Escherichia coli Cu(I)-translocating P-type ATPase. Proc Natl Acad Sci U S A 97(2):652–656
Roggo C, van der Meer JR (2017) Miniaturized and integrated whole cell living bacterial sensors in field applicable autonomous devices. Curr Opin Biotechnol 45:24–33. https://doi.org/10.1016/j.copbio.2016.11.023
Sabermahani F, Taher MA (2014) Determination of ultra trace amounts of copper by a multi-injection technique of electrothermal atomic absorption spectrometry after using solid-phase extraction. J AOAC Int 97(6):1713–1718
Selifonova O, Burlage R, Barkay T (1993) Bioluminescent sensors for detection of bioavailable Hg(II) in the environment. Appl Environ Microbiol 59(9):3083–3090
Singh A, Kumar D, Gaur JP (2008) Removal of Cu(II) and Pb(II) by Pithophora oedogonia: sorption, desorption and repeated use of the biomass. J Hazard Mater 152(3):1011–1019. https://doi.org/10.1016/j.jhazmat.2007.07.07
Stoyanov JV, Hobman JL, Brown NL (2001) CueR (YbbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. Mol Microbiol 39(2):502–511
Thompson CM, Ellwood MJ, Wille M (2013) A solvent extraction technique for the isotopic measurement of dissolved copper in seawater. Anal Chim Acta 775:106–113. https://doi.org/10.1016/j.aca.2013.03.020
Trang PT, Berg M, Viet PH, Van Mui N, Van Der Meer JR (2005) Bacterial bioassay for rapid and accurate analysis of arsenic in highly variable groundwater samples. Environ Sci Technol 39(19):7625–7630
Wang D, Gao Y, Larsson K, Lin W (2016) Speciation of dissolved copper in human impacted freshwater and saltwater lakes. Environ Sci Pollut Res Int 23(11):10832–10840. https://doi.org/10.1007/s11356-016-6140-4
Wei W, Liu X, Sun P, Wang X, Zhu H, Hong M, Mao ZW, Zhao J (2014) Simple whole-cell biodetection and bioremediation of heavy metals based on an engineered lead-specific operon. Environ Sci Technol 48(6):3363–3371. https://doi.org/10.1021/es4046567
Yin K, Lv M, Wang Q, Wu Y, Liao C, Zhang W, Chen L (2016) Simultaneous bioremediation and biodetection of mercury ion through surface display of carboxylesterase E2 from Pseudomonas aeruginosa PA1. Water Res 103:383–390. https://doi.org/10.1016/j.watres.2016.07.053
Zaman BT, Bakirdere EG, Kasa NA, Deniz S, Sel S, Chormey DS, Bakirdere S (2018) Development of an efficient and sensitive analytical method for the determination of copper at trace levels by slotted quartz tube atomic absorption spectrometry after vortex-assisted dispersive liquid-liquid microextraction in biota and water samples using a novel ligand. Environ Monit Assess 190(7):437. https://doi.org/10.1007/s10661-018-6735-y
Funding
This work was supported by the National High Technology Research and Development Program of China (2014AA06A514), the Key Discipline of Zhejiang Province in Medical Technology (First Class, Category A), and the Science and Technology Project of Wenzhou (S20170016).
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Wang, W., Jiang, F., Wu, F. et al. Biodetection and bioremediation of copper ions in environmental water samples using a temperature-controlled, dual-functional Escherichia coli cell. Appl Microbiol Biotechnol 103, 6797–6807 (2019). https://doi.org/10.1007/s00253-019-09984-9
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DOI: https://doi.org/10.1007/s00253-019-09984-9