Journal Home > Volume 11 , Issue 1

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.


menu
Abstract
Full text
Outline
Electronic supplementary material
About this article

Bioluminescent nanopaper for rapid screening of toxic substances

Show Author's information Jie Liu1,2Eden Morales-Narváez1Jahir Orozco1Teresa Vicent3Guohua Zhong2( )Arben Merkoçi1,4( )
Catalan Institute of Nanoscience and Nanotechnology (ICN2)CSIC and the Barcelona Institute of Science and TechnologyCampus UABBellaterraBarcelona08193Spain
Laboratory of Insect ToxicologyKey Laboratory of Pesticide and Chemical BiologyMinistry of EducationSouth China Agricultural UniversityGuangzhou510642China
Departament d'Enginyeria QuímicaUniversitat Autònoma de BarcelonaBellaterraBarcelona08193Spain
ICREAPg. Lluís Companys 2308010Barcelona, Spain

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.

Keywords: bacterial nanocellulose, nanopaper, Aliivibrio fischeri, bioluminescent device, toxicity bioassay

References(38)

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.

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.

3

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

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.

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.

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.

7

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

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.

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.

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.

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.

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.

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.

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.

15

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

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

30

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

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.

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.

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.

34

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

35

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

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.

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.

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.

File
nr-11-1-114_ESM.pdf (2.8 MB)
Publication history
Copyright
Acknowledgements

Publication history

Received: 23 January 2017
Revised: 30 March 2017
Accepted: 01 April 2017
Published: 02 August 2017
Issue date: January 2018

Copyright

© Tsinghua University Press and Springer-Verlag GmbH Germany 2017

Acknowledgements

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).

Return