Skip to main content
SpringerLink
Log in

Bioluminescent nanopaper for rapid screening of toxic substances

  • Research Article
  • Published:
Nano Research Aims and scope Submit manuscript

Abstract

Environmental pollution is threatening human health and ecosystems as a result of modern agricultural techniques and industrial progress. A simple nanopaper-based platform coupled with luminescent bacteria Aliivibrio fischeri (A. fischeri) as a bio-indicator is presented here, for rapid and sensitive evaluation of contaminant toxicity. When exposed to toxicants, the luminescence inhibition of A. fischeri-decorated bioluminescent nanopaper (BLN) can be quantified and analyzed to classify the toxicity level of a pollutant. The BLN composite was characterized in terms of morphology and functionality. Given the outstanding biocompatibility of nanocellulose for bacterial proliferation, BLN achieved high sensitivity with a low cost and simplified procedure compared to conventional instruments for laboratory use only. The broad applicability of BLN devices to environmental samples was studied in spiked real matrices (lake and sea water), and their potential for direct and in situ toxicity screening was demonstrated. The BLN architecture not only survives but also maintains its function during freezing and recycling processes, endowing the BLN system with competitive advantages as a deliverable, ready-to-use device for large-scale manufacturing. The novel luminescent bacteria-immobilized, nanocelullose-based device shows outstanding abilities for toxicity bioassays of hazardous compounds, bringing new possibilities for cheap and efficient environmental monitoring of potential contamination.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Sturm, S.; Hammann, F.; Drewe, J.; Maurer, H. H.; Scholer, A. An automated screening method for drugs and toxic compounds in human serum and urine using liquid chromatography–tandem mass spectrometry. J. Chromatogr. B 2010, 878, 2726–2732.

    Article  Google Scholar 

  2. Maurer, H. H. What is the future of (ultra) high performance liquid chromatography coupled to low and high resolution mass spectrometry for toxicological drug screening? J. Chromatogr. A 2013, 1292, 19–24.

    Article  Google Scholar 

  3. Blasco, C.; Picó, Y. Prospects for combining chemical and biological methods for integrated environmental assessment. TrAC Trend. Anal. Chem. 2009, 28, 745–757.

    Article  Google Scholar 

  4. Yu, D. W.; Liu, J. B.; Sui, Q. W.; Wei, Y. S. Biogas-pH automation control strategy for optimizing organic loading rate of anaerobic membrane bioreactor treating high COD wastewater. Bioresour. Technol. 2016, 203, 62–70.

    Article  Google Scholar 

  5. Oller, I.; Malato, S.; Sánchez-Pérez, J. A.Combination of Advanced Oxidation Processes and biological treatments for wastewater decontamination—A review. Sci. Total Environ. 2011, 409, 4141–4166.

    Article  Google Scholar 

  6. Parvez, S.; Venkataraman, C.; Mukherji, S. A review on advantages of implementing luminescence inhibition test (Vibrio fischeri) for acute toxicity prediction of chemicals. Environ. Int. 2006, 32, 265–268.

    Article  Google Scholar 

  7. Rizzo, L. Bioassays as a tool for evaluating advanced oxidation processes in water and wastewater treatment. Water Res. 2011, 45, 4311–4340.

    Article  Google Scholar 

  8. Farré, M.; Barceló, D. Toxicity testing of wastewater and sewage sludge by biosensors, bioassays and chemical analysis. TrAC Trend. Anal. Chem. 2003, 22, 299–310.

    Article  Google Scholar 

  9. Ma, X. Y.; Wang, X. C.; Ngo, H. H.; Guo, W. S.; Wu, M. N.; Wang, N. Bioassay based luminescent bacteria: Interferences, improvements, and applications. Sci. Total Environ. 2014, 468–469, 1–11.

    Article  Google Scholar 

  10. Xiao, Y. Y.; Araujo, C. D.; Sze, C. C.; Stuckey, D. C. Toxicity measurement in biological wastewater treatment processes: A review. J. Hazard. Mater. 2015, 286, 15–29.

    Article  Google Scholar 

  11. Wieczerzak, M.; Namieśnik, J.; Kudłak, B. Bioassays as one of the Green Chemistry tools for assessing environmental quality: A review. Environ. Int. 2016, 94, 341–361.

    Article  Google Scholar 

  12. Hsieh, C. Y.; Tsai, M. H.; Ryan, D. K.; Pancorbo, O. C. Toxicity of the 13 priority pollutant metals to Vibrio fisheri in the Microtox® chronic toxicity test. Sci. Total Environ. 2004, 320, 37–50.

    Article  Google Scholar 

  13. Joly, P.; Bonnemoy, F.; Charvy, J. C.; Bohatier, J.; Mallet, C. Toxicity assessment of the maize herbicides S-metolachlor, benoxacor, mesotrione and nicosulfuron, and their corresponding commercial formulations, alone and in mixtures, using the Microtox® test. Chemosphere 2013, 93, 2444–2450.

    Article  Google Scholar 

  14. Kralj, M. B.; Trebše, P.; Franko, M. Applications of bioanalytical techniques in evaluating advanced oxidation processes in pesticide degradation. TrAC Trend. Anal. Chem. 2007, 26, 1020–1031.

    Article  Google Scholar 

  15. Isidori, M.; Lavorgna, M.; Nardelli, A.; Pascarella, L.; Parrella, A. Toxic and genotoxic evaluation of six antibiotics on nontarget organisms. Sci. Total Environ. 2005, 346, 87–98.

    Article  Google Scholar 

  16. van der Grinten, E.; Pikkemaat, M. G.; van den Brandhof, E. J.; Stroomberg, G. J.; Kraak, M. H. S. Comparing the sensitivity of algal, cyanobacterial and bacterial bioassays to different groups of antibiotics. Chemosphere 2010, 80, 1–6.

    Article  Google Scholar 

  17. Heidari, F.; Asadollahi, M. A.; Jeihanipour, A.; Kheyrandish, M.; Rismani-Yazdi, H.; Karimi, K. Biobutanol production using unhydrolyzed waste acorn as a novel substrate. RSC Adv. 2016, 6, 9254–9260.

    Article  Google Scholar 

  18. Chang, Z.; Cai, D.; Wang, Y.; Chen, C. J.; Fu, C. H.; Wang, G. Q.; Qin, P. Y.; Wang, Z.; Tan, T. W. Effective multiple stages continuous acetone–butanol–ethanol fermentation by immobilized bioreactors: Making full use of fresh corn stalk. Bioresour. Technol. 2016, 205, 82–89.

    Article  Google Scholar 

  19. Tang, Y. N.; Werth, C. J.; Sanford, R. A.; Singh, R.; Michelson, K.; Nobu, M.; Liu, W. T.; Valocchi, A. J. Immobilization of selenite via two parallel pathways during in situ bioremediation. Environ. Sci. Technol. 2015, 49, 4543–4550.

    Article  Google Scholar 

  20. Liu, J.; Chen, S. H.; Ding, J.; Xiao, Y.; Han, H. T.; Zhong, G. H. Sugarcane bagasse as support for immobilization of Bacillus pumilus HZ-2 and its use in bioremediation of mesotrione-contaminated soils. Appl. Microbiol. Biotechnol. 2015, 99, 10839–10851.

    Article  Google Scholar 

  21. Morales-Narváez, E.; Golmohammadi, H.; Naghdi, T.; Yousefi, H.; Kostiv, U.; Horák, D.; Pourreza, N.; Merkoçi, A. Nanopaper as an optical sensing platform. ACS Nano 2015, 9, 7296–7305.

    Article  Google Scholar 

  22. Klemm, D.; Kramer, F.; Moritz, S.; Lindström, T.; Ankerfors, M.; Gray, D.; Dorris, A. Nanocelluloses: A new family of nature-based materials. Angew. Chem., Int. Ed. 2011, 50, 5438–5466.

    Article  Google Scholar 

  23. Heli, B.; Morales-Narváez, E.; Golmohammadi, H.; Ajji, A.; Merkoçi, A. Modulation of population density and size of silver nanoparticles embedded in bacterial cellulose via ammonia exposure: Visual detection of volatile compounds in a piece of plasmonic nanopaper. Nanoscale 2016, 8, 7984–7991.

    Article  Google Scholar 

  24. Mertaniemi, H.; Escobedo-Lucea, C.; Sanz-Garcia, A.; Gandía, C.; Mäkitie, A.; Partanen, J.; Ikkala, O.; Yliperttula, M. Human stem cell decorated nanocellulose threads for biomedical applications. Biomaterials 2016, 82, 208–220.

    Article  Google Scholar 

  25. Xiong, G. Y.; Luo, H. L.; Zhu, Y.; Raman, S.; Wan, Y. Z. Creation of macropores in three-dimensional bacterial cellulose scaffold for potential cancer cell culture. Carbohyd. Polym. 2014, 114, 553–557.

    Article  Google Scholar 

  26. Bose, J. L.; Kim, U.; Bartkowski, W.; Gunsalus, R. P.; Overley, A. M.; Lyell, N. L.; Visick, K. L.; Stabb, E. V. Bioluminescence in Vibrio fischeri is controlled by the redox-responsive regulator ArcA. Mol. Microbiol. 2007, 65, 538–553.

    Article  Google Scholar 

  27. de la Escosura-Muñiz, A.; Chunglok, W.; Surareungchai, W.; Merkoçi, A. Nanochannels for diagnostic of thrombin-related diseases in human blood. Biosens. Bioelectron. 2013, 40, 24–31.

    Article  Google Scholar 

  28. Villa, S.; Vighi, M.; Finizio, A. Experimental and predicted acute toxicity of antibacterial compounds and their mixtures using the luminescent bacterium Vibrio fischeri. Chemosphere 2014, 108, 239–244.

    Article  Google Scholar 

  29. Galloway, W. R. J. D.; Hodgkinson, J. T.; Bowden, S. D.; Welch, M.; Spring, D. R. Quorum sensing in gram-negative bacteria: Small-molecule modulation of AHL and AI-2 quorum sensing pathways. Chem. Rev. 2011, 111, 28–67.

    Article  Google Scholar 

  30. Ng, W. L.; Bassler, B. L. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 2009, 43, 197–222.

    Article  Google Scholar 

  31. Cacicedo, M. L.; León, I. E.; Gonzalez, J. S.; Porto, L. M.; Alvarez, V. A.; Castro, G. R. Modified bacterial cellulose scaffolds for localized doxorubicin release in human colorectal HT-29 cells. Colloid. Surface. B 2016, 140, 421–429.

    Article  Google Scholar 

  32. Favi, P. M.; Ospina, S. P.; Kachole, M.; Gao, M.; Atehortua, L.; Webster, T. J. Preparation and characterization of biodegradable nano hydroxyapatite–bacterial cellulose composites with well-defined honeycomb pore arrays for bone tissue engineering applications. Cellulose 2016, 23, 1263–1282.

    Article  Google Scholar 

  33. Svensson, A.; Nicklasson, E.; Harrah, T.; Panilaitis, B.; Kaplan, D. L.; Brittberg, M.; Gatenholm, P. Bacterial cellulose as a potential scaffold for tissue engineering of cartilage. Biomaterials 2005, 26, 419–431.

    Article  Google Scholar 

  34. Stebbing, A. R. D. Hormesis—The stimulation of growth by low levels of inhibitors. Sci. Total Environ. 1982, 22, 213–234.

    Article  Google Scholar 

  35. Calabrese, E. J.; Baldwin, L. A.Hormesis: The dose-response revolution. Annu. Rev. Pharmacol. Toxicol. 2003, 43, 175–197.

    Article  Google Scholar 

  36. Donnez, J.; Martinez-Madrid, B.; Jadoul, P.; Van Langendonckt, A.; Demylle, D.; Dolmans, M. M. Ovarian tissue cryopreservation and transplantation: Areview. Hum. Reprod. Update 2006, 12, 519–535.

    Article  Google Scholar 

  37. Kovalevsky, G.; Carney, S. M.; Morrison, L. S.; Boylan, C. F.; Neithardt, A. B.; Feinberg, R. F.Should embryos developing to blastocysts on day 7 be cryopreserved and transferred: An analysis of pregnancy and implantation rates. Fertil. Steril. 2013, 100, 1008–1012.

    Article  Google Scholar 

  38. Subbarayan, K.; Rolletschek, H.; Senula, A.; Ulagappan, K.; Hajirezaei, M. R.; Keller, E. R. J.Influence of oxygen deficiency and the role of specific amino acids in cryopreservation of garlic shoot tips. BMC Biotechnol. 2015, 15, 40.

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the European Commission Program, H2020-WATER, INTCATCH Project (No. 689341). ICN2 acknowledges support from the Severo Ochoa Program (MINECO, Grant SEV-2013-0295). The Nanobiosensors and Bioelectronics Group acknowledges the support from the Generalitat de Cataluña (Grant 2014 SGR 260). Jie Liu acknowledges the support from China Scholarship Council (CSC).

Author information

Authors and Affiliations

  1. Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and the Barcelona Institute of Science and Technology, Campus UAB, Bellaterra, Barcelona, 08193, Spain

    Jie Liu, Eden Morales-Narváez, Jahir Orozco & Arben Merkoçi

  2. Laboratory of Insect Toxicology, Key Laboratory of Pesticide and Chemical Biology, Ministry of Education, South China Agricultural University, Guangzhou, 510642, China

    Jie Liu & Guohua Zhong

  3. Departament d’Enginyeria Química, Universitat Autònoma de Barcelona, Bellaterra, Barcelona, 08193, Spain

    Teresa Vicent

  4. ICREA, Pg. Lluís Companys 23, 08010, Barcelona, Spain

    Arben Merkoçi

Authors
  1. Jie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eden Morales-Narváez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jahir Orozco
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Teresa Vicent
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guohua Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Arben Merkoçi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Guohua Zhong or Arben Merkoçi.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, J., Morales-Narváez, E., Orozco, J. et al. Bioluminescent nanopaper for rapid screening of toxic substances. Nano Res. 11, 114–125 (2018). https://doi.org/10.1007/s12274-017-1610-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12274-017-1610-7

Keywords

Search

Navigation