Heavy metal whole-cell biosensors using eukaryotic microorganisms: An updated critical review

Frontiers in Microbiology

Volumn 6, Issue FEB, 2015, Pages

  Gutiérrez, Juan C ^a   Amaro, Francisco ^a   Martín González, Ana ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Bioassays; Biosensors; Ciliates; Eukaryotic microorganisms; Heavy metals; Microalgae; Yeasts

Indexed keywords

HEAVY METAL;

BIOSENSOR; CHLAMYDOMONAS; ENVIRONMENTAL MONITORING; GENE EXPRESSION; GENETIC ANALYSIS; GROWTH RATE; MORTALITY; NONHUMAN; PROMOTER REGION; REPORTER GENE; REVIEW; SACCHAROMYCES CEREVISIAE; SENSITIVITY ANALYSIS; TETRAHYMENA THERMOPHILA; WHOLE CELL BIOSENSOR;

CHLAMYDOMONAS; CILIOPHORA; EUKARYOTA; MYXOZOA; SACCHAROMYCES CEREVISIAE; TETRAHYMENA THERMOPHILA;

EID: 84927561602     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00048     Document Type: Review

References (42)

1. Aksmann, A., Pokora, W., Bascik-Remisiewicz, A., Dettlaff-Pokora, A., Wielgomas, B., Dziadziusko, M., et al. (2014). Time-dependent changes in antioxidative enzyme expression and photosynthetic activity of Chlamydomonas reinhardtii cells under acute exposure to cadmium and anthracene. Ecotoxicol. Environ. Saf. 110C, 31-40. doi: 10.1016/j.ecoenv.2014.08.005.
2. Amaro, F., Turkewitz, A. P., Martin-Gonzalez, A., and Gutiérrez, J. C. (2011). Whole-cell biosensors for detection of heavy metal ions in environmental samples based on metallothionein promoters from Tetrahymena thermophila. Microb. Biotechnol. 4, 513-522. doi: 10.1111/j.1751-7915.2011.00252.x.
3. Amaro, F., Turkewitz, A. P., Martin-Gonzalez, A., and Gutiérrez, J. C. (2014). Functional GFP-metallothionein fusion protein from Tetrahymena thermophila: a potential whole-cell biosensor for monitoring heavy metal pollution and a cell model to study metallothionein overproduction effects. Biometals 27, 195-205. doi: 10.1007/s10534-014-9704-0.
4. Aury, J. M., Jaillon, O., Duret, L., Noel, B., Jubin, C., Porcel, B. M., et al. (2006). Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444, 171-178. doi: 10.1038/nature05230.
5. Baronian, K. H. R. (2004). The use of yeast and moulds as sensing elements in biosensors. Biosens. Bioelectron. 19, 953-962. doi: 10.1016/j.bios.2003.09.010.
6. Belkin, S. (2003). Microbial whole-cell sensing systems of environmental pollutants. Curr. Opin. Microbiol. 6, 206-212. doi: 10.1016/S1369-5274(03)00059-6.
7. Chouteau, C., Dzyadevych, S., Chovelon, J-M., and Durrieu, C. (2004). Development of novel conductometric biosensors based on immobilised whole cell Chlorella vulgaris microalgae. Biosens. Bioelectron. 19, 1089-1096. doi: 10.1016/j.bios.2003.10.012.
8. Corbisier, P., van der Lelie, D., Borremans, B., Provoost, A., de Lorenzo, V., Brown, N. L., et al. (1999). Whole cell-and protein-based biosensors for the detection of bioavailable heavy metals in environmental samples. Anal. Chim. Acta 387, 235-244. doi: 10.1016/S0003-2670(98)00725-9.
9. De Schamphelaere, K. A. C., Nys, C., and Janssen, C. R. (2014). Toxicity of lead (Pb) to freshwater green algae: development and validation of a bioavailability model and inter-species sensitivity comparison. Aquat. Toxicol. 155, 348-359. doi: 10.1016/j.aquatox.2014.07.008.
10. Díaz, S., Amaro, F., Rico, D., Campos, V., Benitez, L., Martin-Gonzalez, A., et al. (2007). Tetrahymena metallothioneins fall into two discrete subfamilies. PLoS ONE 2:e291. doi: 10.1371/journal.pone.0000291.
11. Eisen, J. A., Coyne, R. S., Wu, M., Wu, D., Thiaragarajan, M., Wortman, J. R., et al. (2006). Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol. 4:e286. doi: 10.1371/journal.pbio.0040286.
12. Fairbrother, A., Wenstel, R., Sappington, K., and Wood, W. (2007). Framework for metals risk assessment. Ecotoxicol. Environ. Saf. 68, 145-227. doi: 10.1016/j.ecoenv.2007.03.015.
13. Greer, L. F., and Szalay, A. A. (2002). Imaging of light emission from the expression of luciferases in living cells and organisms: a review. Luminescence 17, 43-74. doi: 10.1002/bio.676.
14. Gu, M. B., Mitchell, R. J., and Kim, B. C. (2004). Whole-cell-based biosensors for environmental biomonitoring and application. Adv. Biochem. Eng. Biotechnol. 87, 269-305. doi: 10.1007/b13533.
15. Gutiérrez, J. C., Amaro, F., Diaz, S., de Francisco, P., Cubas, L. L., and Martin-Gonzalez, A. (2011). Ciliate metallothioneins: unique microbial eukaryotic heavy-metal-binder molecules. J. Biol. Inorg. Chem. 16, 1025-1034. doi: 10.1007/s00775-011-0820-9.
16. Gutiérrez, J. C., Martin-Gonzalez, A., Diaz, S., Amaro, F., Ortega, R., Gallego, A., et al. (2008). "Ciliates as cellular tools to study the eukaryotic cell-heavy metal interactions, " in Heavy Metal Pollution, eds S. E. Brown and W. C. Welton (New York, NY: Nova Science Publishers), 1-44.
17. Gutiérrez, J. C., Martin-Gonzalez, A., Diaz, S., and Ortega, R. (2003). Ciliate as potential source of cellular and molecular biomarker/biosensors for heavy metal pollution. Eur. J. Protistol. 39, 461-467. doi: 10.1078/0932-4739-00021.
18. Hill, M. K. (2004). Understanding Environmental Pollution. A Primer. Cambridge: Cambridge University Press.
19. Ivask, A., Rolova, T., and Kahru, A. (2009). A suite of recombinant luminescent bacterial strains for the quantification of bioavailable heavy metals and toxicity testing. BMC Biotechnol. 9:41. doi: 10.1186/1472-6750-9-41.
20. Kröger, S., and Law, R. J. (2005). Biosensors for marine applications. We all need the sea, but does the sea need biosensors? Biosens. Bioelectron. 20, 1903-1913. doi: 10.1016/j.bios.2004.08.036.
21. Lagido, C., Pettitt, J., Porter, A. J., Paton, G. I., and Glover, L. A. (2001). Development and application of bioluminescent Caenorhabditis elegans as multicellular eukaryotic biosensors. FEBS Lett. 493, 36-39. doi: 10.1016/S0014-5793(01)02271-2.
22. Lambreva, M. D., Giardi, M. T., Rambaldi, I., Antonacci, A., Pastorelli, S., Bertalan, I., et al. (2013). A powerful molecular engineering tool provided efficient Chlamydomonas mutants as bio-sensing elements for herbicides detection. PLoS ONE 8:e61851. doi: 10.1371/journal.pone.0061851.
23. Leonard, S. S., Harris, G. K., and Shi, X. (2004). Metal-induced oxidative stress and signal transduction. Free Radic. Biol. Med. 12, 1921-1942. doi: 10.1016/j.freeradbiomed.2004.09.010.
24. Magrisso, S., Erel, Y., and Belkin, S. (2008). Microbial reporters of metal bioavailability. Microb. Biotechnol. 1, 320-330. doi: 10.1111/j.1751-7915.2008.00022.x.
25. Martin-Gonzalez, A., Diaz, S., Jareño, C., and Gutiérrez, J. C. (1999). The use of protists in ecotoxicology. Recent Res. Dev. Microbiol. 3, 93-111.
26. Park, J-N., Sohn, M. J., Oh, D-B., Kwon, O., Rhee, S. K., Hur, C-G., et al. (2007). Identification of the cadmium-inducible Hansenula polymorpha SEO1 gene promoter by transcriptome analysis and its application to whole-cell heavy metal detection systems. Appl. Environ. Microbiol. 73, 5990-6000. doi: 10.1128/AEM.00863-07.
27. Peña-Vázquez, E., Perez-Conde, C., Costas, E., and Moreno-Bondi, M. C. (2010). Development of a microalgal PAM test method for Cu(II) in waters: comparison of using spectrofluorometry. Ecotoxicology 19, 1059-1065. doi: 10.1007/s10646-010-0487-y.
28. Preston, S., Coad, N., Townend, J., Killham, K., and Paton, G. I. (2000). Biosensing the acute toxicity of metal interactions: are they additive, synergistic or antagonistic? Environ. Toxicol. Chem. 19, 775-780. doi: 10.1002/etc.5620190332.
29. Pulido, M. D., and Parrish, A. R. (2003). Metal-induced apoptosis: mechanisms. Mutat. Res. 533, 227-241. doi: 10.1016/j.mrfmmm.2003.07.015.
30. Robbens, J., Maras, M., Laureyn, W., Blust, R., and De Coen, W. (2005). "Whole cell biosensors for (eco)toxicity screening: alternatives for the future, " in Technical Proceedings of the 2005 NSTI Nanotechnology Conference and Trade Show, Vol. 1 (Austin, TX: Nano Science and Technology Institute), 497-500.
31. Roda, A., Roda, B., Cevenini, L., Michelini, E., Mezzanotte, L., Reschiglian, P., et al. (2011). Analytical strategies for improving the robustness and reproducibility of bioluminescent microbial bioreporters. Anal. Bioanal. Chem. 401, 201-211. doi: 10.1007/s00216-011-5091-3.
32. Shetty, R. S., Deo, S. K., Liu, Y., and Daunert, S. (2004). Fluorescence-based sensing system for copper using genetically engineered living yeast cells. Biotechnol. Bioeng. 88, 664-670. doi: 10.1002/bit.20331.
33. Shitanda, I., Takada, K., Sakai, Y., and Tatsuma, T. (2005). Amperometric biosensing systems based on motility and gravitaxis of flagellate algae for aquatic risk assessment. Anal. Chem. 77, 6715-6718. doi: 10.1021/ac050894b.
34. Terziyska, A., Waltschewa, L., and Venkov, P. (2000). A new sensitive test based on yeast cells for studying environmental pollution. Environ. Pollut. 109, 43-52. doi: 10.1016/S0269-7491(99)00237-7.
35. Tom-Petersen, A., Hosbond, C., and Nybroe, O. (2001). Identification of copper-induced genes in Pseudomonas fluorescens and use of a reporter strain to monitor bioavailable copper in soil. FEMS Microbiol. Ecol. 38, 59-65. doi: 10.1111/j.1574-6941.2001.tb00882.x.
36. Valko, M., Morris, H., and Cronin, M. T. (2005). Metals, toxicity and oxidative stress. Curr. Med. Chem. 12, 1161-1208. doi: 10.2174/0929867053764635.
37. Valko, M., Rhodes, C. J., Moncol, J., Izakovic, M., and Mazur, M. (2006). Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 160, 1-40. doi: 10.1016/j.cbi.2005.12.009.
38. Van der Meer, J. R., and Belkin, S. (2010). Where microbiology meets microengineering: design and applications of reporter bacteria. Nat. Rev. Microbiol. 8, 511-522. doi: 10.1038/nrmicro2392.
39. Van der Meer, J. R., Tropel, D., and Jaspers, M. (2004). Illuminating the detection chain of bacterial bioreporters. Environ. Microbiol. 6, 1005-1020. doi: 10.1111/j.1462-2920.2004.00655.x.
40. Védrine, C., Leclerc, J. C., Durrieu, C., and Tran-Minh, C. (2003). Optical whole-cell biosensors using Chlorella vulgaris designed for monitoring herbicides. Biosens. Bioelectron. 18, 457-463. doi: 10.1016/S0956-5663(02)00157-4.
41. Walmsley, R. M., and Keenan, P. (2000). The eukaryotic alternative: advantages of using yeasts in place of bacteria in microbial biosensor development. Biotechnol. Bioprocess Eng. 5, 387-394. doi: 10.1007/BF02931936.
42. Yagi, K. (2007). Applications of whole-cell bacterial sensors in biotechnology and environmental science. Appl. Microbiol. Biotechnol. 73, 1251-1258. doi: 10.1007/s00253-006-0718-6.