{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,20]],"date-time":"2026-06-20T02:12:31Z","timestamp":1781921551235,"version":"3.54.5"},"reference-count":46,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2025,5,29]],"date-time":"2025-05-29T00:00:00Z","timestamp":1748476800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Jiangsu Distinguished Professor Project","award":["RC20240909"],"award-info":[{"award-number":["RC20240909"]}]},{"name":"Jiangsu Distinguished Professor Project","award":["22JDG033"],"award-info":[{"award-number":["22JDG033"]}]},{"DOI":"10.13039\/501100019226","name":"Jiangsu University Foundation","doi-asserted-by":"publisher","award":["RC20240909"],"award-info":[{"award-number":["RC20240909"]}],"id":[{"id":"10.13039\/501100019226","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100019226","name":"Jiangsu University Foundation","doi-asserted-by":"publisher","award":["22JDG033"],"award-info":[{"award-number":["22JDG033"]}],"id":[{"id":"10.13039\/501100019226","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biosensors"],"abstract":"<jats:p>Heavy metal contamination in livestock and poultry farm wastewater poses significant risks to both the environment and human health, so it is critical to accurately and rapidly quantify heavy metal ion concentrations in water. This research develops a bioelectric active hydrogel sensor for detecting heavy metal ions in livestock wastewater. The sensor integrates microbial surface display technology with graphene hydrogel, displaying glucose oxidase (GOx) on the surface of yeast cells, and covalently incorporating it into the graphene hydrogel through the bio-reduction activity of metal-reducing bacteria, enhancing its electrochemical performance. The sensor demonstrates excellent sensitivity and stability in detecting Cu2+, with a detection limit for Cu2+ of 17.0 \u00b5M. This sensor is also applicable for detecting Zn2+ in wastewater. When various heavy metal ions coexist in the solution, they exert a more pronounced inhibitory effect on enzyme activity. Consequently, the sensor can be employed to assess the overall heavy metal content in water samples. In the detection of Cu2+ in real livestock and poultry wastewater, the recovery rate of the graphene hydrogel electrode ranged from 88% to 106.5%, indicating that the sensor holds significant potential for application in actual sample analysis.<\/jats:p>","DOI":"10.3390\/bios15060341","type":"journal-article","created":{"date-parts":[[2025,5,29]],"date-time":"2025-05-29T04:46:38Z","timestamp":1748493998000},"page":"341","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["A Bioelectric Active Hydrogel Sensor for Trace Detection of Heavy Metal Ions in Livestock and Poultry Farm Wastewater"],"prefix":"10.3390","volume":"15","author":[{"given":"Heng-Chi","family":"Liu","sequence":"first","affiliation":[{"name":"Institute for Energy Research, School of Environment and Safety Engineering, Jiangsu University, 301 Xuefu Road, Zhenjiang 212013, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jia-Xin","family":"Du","sequence":"additional","affiliation":[{"name":"Institute for Energy Research, School of Environment and Safety Engineering, Jiangsu University, 301 Xuefu Road, Zhenjiang 212013, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jie","family":"Wang","sequence":"additional","affiliation":[{"name":"Institute for Energy Research, School of Environment and Safety Engineering, Jiangsu University, 301 Xuefu Road, Zhenjiang 212013, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junying","family":"Liu","sequence":"additional","affiliation":[{"name":"Institute for Energy Research, School of Environment and Safety Engineering, Jiangsu University, 301 Xuefu Road, Zhenjiang 212013, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-0390-6760","authenticated-orcid":false,"given":"Luyu","family":"Yang","sequence":"additional","affiliation":[{"name":"Institute for Energy Research, School of Environment and Safety Engineering, Jiangsu University, 301 Xuefu Road, Zhenjiang 212013, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1216-5163","authenticated-orcid":false,"given":"Yang-Chun","family":"Yong","sequence":"additional","affiliation":[{"name":"Institute for Energy Research, School of Environment and Safety Engineering, Jiangsu University, 301 Xuefu Road, Zhenjiang 212013, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,5,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Rajendran, S., Priya, T.A.K., Khoo, K.S., Hoang, T.K.A., Ng, H.-S., Munawaroh, H.S.H., Karaman, C., Orooji, Y., and Show, P.L. (2022). A critical review on various remediation approaches for heavy metal contaminants removal from contaminated soils. Chemosphere, 287.","DOI":"10.1016\/j.chemosphere.2021.132369"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Shi, J., Zhao, D., Ren, F., and Huang, L. (2023). Spatiotemporal variation of soil heavy metals in China: The pollution status and risk assessment. Sci. Total Environ., 871.","DOI":"10.1016\/j.scitotenv.2023.161768"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Han, F., Huang, X., and Teye, E. (2019). Novel prediction of heavy metal residues in fish using a low-cost optical electronic tongue system based on colorimetric sensors array. J. Food Process Eng., 42.","DOI":"10.1111\/jfpe.12983"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Liu, S., Sun, Q., Xu, N., Wang, Y., Li, Y., Li, J., Li, Z., Rajput, V.D., Minkina, T., and Kong, X. (2025). Recent advances in the treatment of heavy\/precious metal pollution, resource recovery and reutilization: Progress and perspective. Coord. Chem. Rev., 523.","DOI":"10.1016\/j.ccr.2024.216268"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"7215","DOI":"10.1039\/D1CC00983D","article-title":"Electrochemical detection of heavy metal ions in water","volume":"57","author":"Ding","year":"2021","journal-title":"Chem. Commun."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Li, R., Wu, H., Ding, J., Fu, W., Gan, L., and Li, Y. (2017). Mercury pollution in vegetables, grains and soils from areas surrounding coal-fired power plants. Sci. Rep., 7.","DOI":"10.1038\/srep46545"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1591","DOI":"10.1016\/j.scitotenv.2017.06.030","article-title":"Soil contamination with cadmium, consequences and remediation using organic amendments","volume":"601\u2013602","author":"Khan","year":"2017","journal-title":"Sci. Total Environ."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Feng, L., Yan, H., Dai, C., Xu, W., Gu, F., Zhang, F., Li, T., Xian, J., He, X., and Yu, Y. (2020). The systematic exploration of cadmium-accumulation characteristics of maize kernel in acidic soil with different pollution levels in China. Sci. Total Environ., 729.","DOI":"10.1016\/j.scitotenv.2020.138972"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1016\/j.envpol.2019.03.079","article-title":"Selenium induces changes of rhizosphere bacterial characteristics and enzyme activities affecting chromium\/selenium uptake by pak choi (Brassica campestris L. ssp. Chinensis Makino) in chromium contaminated soil","volume":"249","author":"Cai","year":"2019","journal-title":"Environ. Pollut."},{"key":"ref_10","unstructured":"(1996). Integrated Wastewater Discharge Standard (Standard No. GB 8978\u20131996)."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Gujre, N., Rangan, L., and Mitra, S. (2021). Occurrence, geochemical fraction, ecological and health risk assessment of cadmium, copper and nickel in soils contaminated with municipal solid wastes. Chemosphere, 271.","DOI":"10.1016\/j.chemosphere.2021.129573"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Dong, X., Huang, A., He, L., Cai, C., and You, T. (2024). Recent advances in foodborne pathogen detection using photoelectrochemical biosensors: From photoactive material to sensing strategy. Front. Sustain. Food Syst., 8.","DOI":"10.3389\/fsufs.2024.1432555"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"136284","DOI":"10.1016\/j.cej.2022.136284","article-title":"Robust PEDOT:PSS-based hydrogel for highly efficient interfacial solar water purification","volume":"442","author":"Zhao","year":"2022","journal-title":"Chem. Eng. J."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"118364","DOI":"10.1016\/j.desal.2024.118364","article-title":"Photothermal-photocatalytic bifunctional highly porous hydrogel for efficient coherent sewage purification-clean water generation","volume":"597","author":"Xu","year":"2025","journal-title":"Desalination"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Qin, H., Zhao, S., Gong, H., Yu, Z., Chen, Q., Liang, P., and Zhang, D. (2023). Recent Progress in the Application of Metal Organic Frameworks in Surface-Enhanced Raman Scattering Detection. Biosensors, 13.","DOI":"10.3390\/bios13040479"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"214966","DOI":"10.1016\/j.ccr.2022.214966","article-title":"Recent advancement in graphene quantum dots based fluorescent sensor: Design, construction and bio-medical applications","volume":"478","author":"Li","year":"2023","journal-title":"Coord. Chem. Rev."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1016\/j.procbio.2012.02.007","article-title":"Construction of a bacterial biosensor for zinc and copper and its application to the development of multifunctional heavy metal adsorption bacteria","volume":"47","author":"Ravikumar","year":"2012","journal-title":"Process Biochem."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Ashrafi, A.M., S\u00fds, M., Sedl\u00e1\u010dkov\u00e1, E., Shaaban Farag, A., Adam, V., P\u0159ibyl, J., and Richtera, L. (2019). Application of the Enzymatic Electrochemical Biosensors for Monitoring Non-Competitive Inhibition of Enzyme Activity by Heavy Metals. Sensors, 19.","DOI":"10.3390\/s19132939"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"108817","DOI":"10.1016\/j.microc.2023.108817","article-title":"Advances in the application of single-atom nanozymes for heavy metal ion detection, tumor therapy and antimicrobial therapy","volume":"191","author":"Wang","year":"2023","journal-title":"Microchem. J."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Wang, S. (2021). Construction of DNA Biosensors for Mercury (II) Ion Detection Based on Enzyme-Driven Signal Amplification Strategy. Biomolecules, 11.","DOI":"10.3390\/biom11030399"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Sun, G., Wei, X., Zhang, D., Huang, L., Liu, H., and Fang, H. (2023). Immobilization of Enzyme Electrochemical Biosensors and Their Application to Food Bioprocess Monitoring. Biosensors, 13.","DOI":"10.20944\/preprints202308.1310.v1"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"842","DOI":"10.1590\/S1516-8913201401358","article-title":"Immobilization of Beauveria bassiana Lipase on Silica Gel by Physical Adsorption","volume":"57","author":"Sugahara","year":"2014","journal-title":"Braz. Arch. Biol. Technol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1016\/j.snb.2007.11.049","article-title":"Inhibitive determination of metal ions by an amperometric glucose oxidase biosensor","volume":"131","author":"Guascito","year":"2008","journal-title":"Sens. Actuators B Chem."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"15063","DOI":"10.3390\/s121115063","article-title":"Indirect Determination of Mercury Ion by Inhibition of a Glucose Biosensor Based on ZnO Nanorods","volume":"12","author":"Chey","year":"2012","journal-title":"Sensors"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1016\/j.snb.2004.09.005","article-title":"Screen-printed disposable urease-based biosensors for inhibitive detection of heavy metal ions","volume":"106","author":"Tymecki","year":"2005","journal-title":"Sens. Actuators B Chem."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"7910","DOI":"10.1021\/acs.jafc.1c02056","article-title":"Construction of Multienzyme Co-immobilized Hybrid Nanoflowers for an Efficient Conversion of Cellulose into Glucose in a Cascade Reaction","volume":"69","author":"Han","year":"2021","journal-title":"J. Agric. Food Chem."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1016\/j.foodchem.2017.07.109","article-title":"Development of a biomimetic enzyme-linked immunosorbent assay based on molecularly imprinted polymers on paper for the detection of carbaryl","volume":"240","author":"Zhang","year":"2018","journal-title":"Food Chem."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.tibtech.2010.11.003","article-title":"Decorating microbes: Surface display of proteins on Escherichia coli","volume":"29","author":"Winter","year":"2011","journal-title":"Trends Biotechnol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1007\/s00253-012-4175-0","article-title":"Recent developments in yeast cell surface display toward extended applications in biotechnology","volume":"95","author":"Tanaka","year":"2012","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Lozan\u010di\u0107, M., Sk Hossain, A., Mr\u0161a, V., and Tepari\u0107, R. (2019). Surface Display\u2014An Alternative to Classic Enzyme Immobilization. Catalysts, 9.","DOI":"10.3390\/catal9090728"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2179","DOI":"10.1002\/jsfa.13988","article-title":"High-throughput screening and identification of lignin peroxidase based on spore surface display of Bacillus subtilis","volume":"105","author":"Shi","year":"2025","journal-title":"J. Sci. Food Agric."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1128\/AEM.02463-09","article-title":"Enhanced Display of Lipase on the Escherichia coli Cell Surface, Based on Transcriptome Analysis","volume":"76","author":"Han","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1021\/bp060333l","article-title":"Identification of Peptide Ligands Facilitating Nanoparticle Attachment to Erythrocytes","volume":"23","author":"Hall","year":"2008","journal-title":"Biotechnol. Prog."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Ding, J., Liu, Y., Gao, Y., Zhang, C., Wang, Y., Xu, B., Yang, Y., Wu, Q., and Huang, Z. (2022). Biodegradation of \u03bb-cyhalothrin through cell surface display of bacterial carboxylesterase. Chemosphere, 289.","DOI":"10.1016\/j.chemosphere.2021.133130"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.bios.2013.07.021","article-title":"Co-immobilization of glucoamylase and glucose oxidase for electrochemical sequential enzyme electrode for starch biosensor and biofuel cell","volume":"51","author":"Lang","year":"2014","journal-title":"Biosens. Bioelectron."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1021\/acs.est.8b05275","article-title":"Biocatalytic Degradation of Parabens Mediated by Cell Surface Displayed Cutinase","volume":"53","author":"Zhu","year":"2018","journal-title":"Environ. Sci. Technol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1016\/j.biortech.2013.02.069","article-title":"Effect of shear rate on the response of microbial fuel cell toxicity sensor to Cu(II)","volume":"136","author":"Shen","year":"2013","journal-title":"Bioresour. Technol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"141544","DOI":"10.1016\/j.scitotenv.2020.141544","article-title":"On-line monitoring of repeated copper pollutions using sediment microbial fuel cell based sensors in the field environment","volume":"748","author":"Liu","year":"2020","journal-title":"Sci. Total Environ."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.talanta.2016.04.011","article-title":"Glutathione modified screen-printed carbon nanofiber electrode for the voltammetric determination of metal ions in natural samples","volume":"155","author":"Serrano","year":"2016","journal-title":"Talanta"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"5610","DOI":"10.1039\/D1AN01012C","article-title":"In situ detection of heavy metal ions in sewage with screen-printed electrode-based portable electrochemical sensors","volume":"146","author":"Bao","year":"2021","journal-title":"Analyst"},{"key":"ref_41","first-page":"872","article-title":"An enzyme biosensor based on beta-galactosidase inhibition for electrochemical detection of cadmium (II) and chromium (VI)","volume":"96","author":"Fourou","year":"2016","journal-title":"Int. J. Environ. Anal. Chem."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1016\/j.snb.2011.02.040","article-title":"Sensing of lead ions using glutathione mediated end to end assembled gold nanorod chains","volume":"156","author":"Durgadas","year":"2011","journal-title":"Sens. Actuators B-Chem."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2018\/8972549","article-title":"Ion-Imprinted Polymer-Based Receptors for Sensitive and Selective Detection of Mercury Ions in Aqueous Environment","volume":"2018","author":"Yasinzai","year":"2018","journal-title":"J. Sens."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1220","DOI":"10.1016\/j.snb.2017.08.046","article-title":"A miniaturized and flexible cadmium and lead ion detection sensor based on micro-patterned reduced graphene oxide\/carbon nanotube\/bismuth composite electrodes","volume":"255","author":"Xuan","year":"2018","journal-title":"Sens. Actuators B-Chem."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.snb.2011.03.023","article-title":"Detection of heavy metal ions in aqueous solution by P(MBTVBC-co-VIM)-coated QCM","volume":"157","author":"Cao","year":"2011","journal-title":"Sens. Actuators B-Chem."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1007\/s13530-021-00108-3","article-title":"Correction to: Integrated device for colorimetric detection of arsenite using polyethylene glycol capped gold nanoparticles\u2014Lab-on-chip","volume":"13","author":"Shalvi","year":"2021","journal-title":"J. Toxicol. Environ. Health Sci."}],"container-title":["Biosensors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6374\/15\/6\/341\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:42:50Z","timestamp":1760031770000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6374\/15\/6\/341"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,29]]},"references-count":46,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2025,6]]}},"alternative-id":["bios15060341"],"URL":"https:\/\/doi.org\/10.3390\/bios15060341","relation":{},"ISSN":["2079-6374"],"issn-type":[{"value":"2079-6374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,29]]}}}