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  • Print publication year: 2007
  • Online publication date: October 2013

11 - Bioluminescence-based fungal biosensors

from IV - Fungal bioremediation



To apply suitable bioremediation techniques, an understanding of the physical, chemical and biological attributes of an environmental matrix is required. Effective bioremediation is based on optimizing these attributes to enhance the biodegradation of target pollutants. Fundamental to these processes is the concept of bioavailability and bioaccessibility of these pollutants at a suitable and relevant scale (Alexander, 2000; Semple et al., 2004). Environmental analyses are still based on chemical approaches that usually require an exhaustive extraction step prior to chromatographic analysis. This extracted fraction is commonly modelled to assess the portion that may cause harm to a particular target receptor. It is widely acknowledged that modelled values may be appropriate for human risk assessment (though inherently conservative) but yield little information for hazard assessment in a wider ecological or environmental context (Alexander, 2000). Many authors have demonstrated that chemical analysis alone does not provide information regarding the bioavailable fraction of compounds nor about their effects on selected biological receptors (Power et al., 1998; Hansen & Sørensen, 2001; Belkin, 2003; Paton & Killham, 2003). Biological assays are able to complement chemical analysis by considering the effects of all pollutants present in a sample, including those not detected by chemical analysis or those unable to be fitted in a model. Bioassays are used for monitoring the progress of bioremediation because they determine the bioavailable fraction of compounds that in part determines the biodegradability of a compound (Hansen & Sørensen, 2001; Paton & Killham, 2003). However, Semple et al.

Aflalo, C. (1990). Targeting of cloned firefly luciferase to yeast mitochondria. Biochemistry, 29, 4758–66.
Airth, R. L. & Foerster, G. E. (1962). The isolation of catalytic components required for cell-free fungal bioluminescence. Archives of Biochemistry and Biophysics, 97, 567–73.
Alexander, M. (2000). Aging, bioavailability, and overestimation of risk from environmental pollutants. Environmental Science and Technology, 34, 4259–65.
Alkasrawi, M., Nandakumar, R., Margesin, R., Schinner, F. & Mattiasson, B. (1999). A microbial biosensor based on Yarrowia lipolytica for the off-line determination of middle-chain alkanes. Biosensors and Bioelectronics, 14, 723–7.
Alleman, B. C., Logan, B. E. & Gilbertson, R. L. (1992). Toxicity of pentachlorophenol to six species of white rot fungi as a function of chemical dose. Applied and Environmental Microbiology, 58, 4048–50.
Baeumner, A. J. (2003). Biosensors for environmental pollutants and food contaminants. Analytical and Bioanalytical Chemistry, 377, 434–45.
Baronian, K. H. R. (2004). The use of yeast and moulds as sensing elements in biosensors. Biosensors and Bioelectronics, 19, 953–62.
Belkin, S. (2003). Microbial whole-cell sensing systems of environmental pollutants. Current Opinion in Microbiology, 6, 206–12.
Bhattacharyya, J., Read, D., Amos, S., Dooley, S., Killham, K. & Paton, G. I. (2005). Biosensor-based diagnostics of contaminated groundwater: assessment and remediation strategy. Environmental Pollution, 134, 485–92.
Billinton, N., Barker, M. G., Michel, C. E., Knight, A. W., Heyer, W.-D., Goddard, N. J., Fielden, P. R. & Walmsley, R. M. (1998). Development of a green fluorescent protein reporter for a yeast genotoxicity biosensor. Biosensors and Bioelectronics, 13, 831–8.
Blaudez, D., Jacob, C., Turnau, K., Colpaert, J. V., Ahonen-Jonnarth, U., Finlay, R., Botton, B. & Chalot, M. (2000). Differential responses of ectomycorrhizal fungi to heavy metals in vitro. Mycological Research, 104, 1366–71.
Boylan, M., Pelletier, J. & Meighen, E. A. (1989). Fused bacterial luciferase subunits catalyze light emission in eukaryotes and prokaryotes. Journal of Biological Chemistry, 264, 1915–18.
Bundy, J. G., Campbell, C. D. & Paton, G. I. (2001). Comparison of response of six different luminescent bacterial bioassays to bioremediation of five contrasting oils. Journal of Environmental Monitoring, 3, 404–10.
Campanella, L., Favero, G. & Tomassetti, M. (1995). Immobilised yeast cells biosensor for total toxicity testing. The Science of the Total Environment, 171, 227–34.
Campbell, C. D., Paton, G. I., Towers, W., Paterson, E., Dawson, J. C. C., Cameron, C. M., Coull, M. C. & Christie, P. (2001). A biological classification scheme to assess the sensitivity of Scottish and Northern Ireland soils to heavy metals. SNIFFER Report No SR (00) 08.
Chatterjee, J. & Meighen, E. A. (1995). Biotechnological applications of bacterial bioluminescence (lux) genes. Photochemistry and Photobiology, 62, 641–50.
Chaudri, A. M., Knight, B. P., Barbosa-Jefferson, V. L., Preston, S., Paton, G. I., Killham, K., Coad, N., Nicholson, F. A., Chambers, B. J. & McGrath, S. P. (1999). Determination of acute Zn toxicity in pore water from soils previously treated with sewage sludge using bioluminescence assays. Environmental Science and Technology, 33, 1880–5.
Chiu, S. W., Ching, M. L., Fong, K. L. & Moore, D. (1998). Spent oyster mushroom substrate performs better than mushroom mycelia in removing the biocide pentachlorophenol. Mycological Research, 102, 1553–62.
Daunert, S., Barrett, G., Feliciano, J. S., Shetty, R. S., Shrestha, S. & Smith-Spencer, W. (2000). Genetically engineered whole-cell sensing systems: coupling biological recognition with reporter genes. Chemical Reviews, 100, 2705–38.
Dennison, M. J. & Turner, A. P. F. (1995). Biosensors for environmental monitoring. Biotechnology Advances, 13, 1–12.
D'Souza, S. F. (2001). Microbial biosensors. Biosensors and Bioelectronics, 16, 337–53.
Escher, A., O'Kane, D. J., Lee, J. & Szalay, A. A. (1989). Bacterial luciferase αβ fusion protein is fully active as a monomer and highly sensitive in vivo to elevated temperature. Proceedings of the National Academy of Sciences of the United States of America, 86, 6528–32.
Farré, M., Arranz, F., Ribó, J. & Barceló, D. (2004). Interlaboratory study of the bioluminescence inhibition tests for rapid wastewater toxicity assessment. Talanta, 62, 549–58.
Gupta, R. K., Patterson, S. S., Ripp, S., Simpson, M. L. & Sayler, G. S. (2003). Expression of the Photorhabdus luminescens lux genes (luxA, B, C, D, and E) in Saccharomyces cerevisiae. FEMS Yeast Research, 4, 305–13.
Hansen, L. H. & Sørensen, S. J. (2001). The use of whole-cell biosensors to detect and quantify compounds or conditions affecting biological systems. Microbial Ecology, 42, 483–93.
Herring, P. J. (1994). Luminous fungi. Mycologist, 8, 181–3.
Hill, P. J., Rees, C. E. D., Winson, M. K. & Stewart, G. S. A. B. (1993). The application of lux genes. Biotechnology and Applied Biochemistry, 17, 3–14.
Hoiland, K. (1995). Reaction of some decomposer basidiomycetes to toxic elements. Nordic Journal of Botany, 15, 305–18.
Hoiland, K. & Dybdahl, H. G. (1993). A micro-well method for estimating fungal response to metal ions. Response to aluminium by some saprophytic basidiomycetes. Nordic Journal of Botany, 13, 691–6.
Hollis, R. P. (1999). Construction and application of a luminescent eukaryotic biosensor. Ph.D. thesis, University of Aberdeen.
Hollis, R. P., Killham, K. & Glover, L. A. (2000). Design and application of a biosensor for monitoring toxicity of compounds to eukaryotes. Applied and Environmental Microbiology, 66, 1676–9.
Hollis, R. P., Lagido, C., Pettitt, J., Porter, A. J. R., Killham, K., Paton, G. I. & Glover, L. A. (2001). Toxicity of the bacterial luciferase substrate, n-decyl aldehyde, to Saccharomyes cerevisiae and Caenorhabditis elegans. FEBS Letters, 506, 140–2.
Hrenovic, J., Stilinovic, B. & Dvoracek, L. (2005). Use of prokaryotic and eukaryotic biotests to assess toxicity of wastewater from pharmaceutical sources. Acta Chimica Slovenica, 52, 119–25.
Kamzolkina, O. V., Bekker, Z. E. & Egorov, N. S. (1984). Extraction of the luciferin-luciferase system from the fungus Armillaria mellea. Biologicheskiye Nauki, 1, 73–7.
Keane, A., Phoenix, P., Ghoshal, S. & Lau, P. C. K. (2002). Exposing culprit organic pollutants: a review. Journal of Microbiological Methods, 49, 103–19.
Kelly, C. J., Lajoie, C. A., Layton, A. C. & Sayler, G. S. (1999). Bioluminescent reporter bacterium for toxicity monitoring in biological wastewater treatment systems. Water Environment Research, 71, 31–5.
Kirchner, G., Roberts, J. L., Gustafson, G. D. & Ingolia, T. D. (1989). Active bacterial luciferase from a fused gene: expression of a Vibrio harveyi luxAB translational fusion in bacteria, yeast and plant cells. Gene, 81, 349–54.
Koehler, S., Belkin, S. & Schmid, R. D. (2000). Reporter gene bioassays in environmental analysis. Fresenius Journal of Analytical Chemistry, 366, 769–79.
Korpan, Y. I. & El'skaya, A. V. (1995). Microbial sensors: achievements, problems, and prospects. Biochemistry (Moscow), 60, 1517–24.
Kuwabara, S. & Wassink, E. C. (1966). Purification and properties of the active substance of fungal luminescence. In Bioluminescence in Progress, eds. Johnson, F. H. & Haneda, Y.. Princeton: Princeton University Press, pp. 233–45.
Lorang, J. M., Tuori, R. P., Martinez, J. P., Sawyer, T. L., Redman, R. S., Rollins, J. A., Wolpert, T. J., Johnson, K. B., Rodriguez, R. J., Dickman, M. B. & Cuiffeti, L. M. (2001). Green fluorescent protein is lighting up fungal biology. Applied and Environmental Microbiology, 67, 1987–94.
Meighen, E. A. (1991). Molecular biology of bacterial bioluminescence. Microbiological Reviews, 55, 123–42.
Meighen, E. A. (1993). Bacterial bioluminescence: organization, regulation, and application of the lux genes. FASEB Journal, 7, 1016–22.
Mowat, F. S. & Bundy, K. J. (2001). Correlation of field-measured toxicity with chemical concentration and pollutant availability. Environment International, 27, 479–89.
O'Kane, D. J., Lingle, W. L., Porter, D. & Wampler, J. E. (1986). Development and localization of bioluminescence in the fruiting bodies of the mushroom Panellus stypticus. Photochemistry and Photobiology, 43, 100s.
O'Kane, D. J., Lingle, W. L., Porter, D. & Wampler, J. E. (1990). Spectral analysis of bioluminescence of Panellus stypticus. Mycologia, 82, 607–16.
Palmer, G., McFadzean, R., Killham, K., Sinclair, A. & Paton, G. I. (1998). Use of lux-based biosensors for rapid diagnosis of pollutants in arable soils. Chemosphere, 36, 2683–97.
Paton, G. I., Rattray, E. A. S., Campbell, C. D., Cresser, M. S., Glover, L. A., Meeussen, J. C. L. & Killham, K. (1997). Use of genetically modified microbial biosensors for soil ecotoxicity testing. In Biological Indicators of Soil Health and Sustainable Productivity, eds. Pankhurst, C., Doube, B. & Gupta, V.. Wallingford: CAB International, pp. 397–418.
Paton, G. I. & Killham, K. (2003). Intelligent site assessment – a role for ecotoxicology. In Bioremediation: A Critical Review, eds. Head, I. M., Singleton, I. & Milner, M. G.. Wymondham: Horizon Scientific Press, pp. 157–83.
Paton, G. I., Viventsova, R. E., Kumpene, J., Wilson, M. J., Weitz, H. J. & Dawson, J. J. C. (2006). An ecotoxicity assessment of contaminated forest soils from the Kola Peninsula. Science of the Total Environment, 355, 106–17.
Power, M., Meer, J. R., Tchelet, R., Egli, T. & Eggen, R. (1998). Molecular-based methods can contribute to assessments of toxicological risks and bioremediation strategies. Journal of Microbiological Methods, 32, 107–19.
Ramanathan, S., Ensor, M. & Daunert, S. (1997). Bacterial biosensors for monitoring toxic metals. Trends in Biotechnology, 15, 500–6.
Rattray, E. A. S., Prosser, J. I., Killham, K. & Glover, L. A. (1990). Luminescence-based non-extractive technique for in situ detection of Escherichia coli in soil. Applied and Environmental Microbiology, 56, 3368–74.
Ripp, S., Nivens, D. E., Ahn, Y., Werner, C., Jarrell, J. IV, Easter, J. P., Cox, C. D., Burlage, R. S. & Sayler, G. S. (2000). Controlled field release of a bioluminescent genetically engineered microorganism for bioremediation process monitoring and control. Environmental Science and Technology, 34, 846–53.
Sabev, H. A., Handley, P. S. & Robson, G. D. (2004). In situ quantification of biocide efficacy using GFP transformed Aureobasidium pullulans. Journal of Applied Microbiology, 97, 1132–9.
Sanseverino, J., Gupta, R. K., Layton, A. C., Patterson, S. S., Rip, S. A., Saidak, L., Simpson, M. L., Schultz, T. W. & Sayler, G. S. (2005). Use of Saccharomyces cerevisiae BLYES expressing bacterial bioluminescence for rapid, sensitive detection of estrogenic compounds. Applied and Environmental Microbiology, 71, 4455–60.
Semple, K. T., Doick, K. J., Jones, K. C., Burauel, P., Craven, A. & Harms, H. (2004). Defining bioavailability and bioaccessibility of contaminated soil and sediment is complicated. Environmental Science and Technology, 38, 209A–232A.
Shimomura, O. (1992). Role of superoxide dismutase in regulating the light emission of luminescent fungi. Journal of Experimental Botany, 43, 1519–25.
Sousa, S., Duffy, C., Weitz, H., Glover, L. A., Baer, E., Henkler, R. & Killham, K. (1998). Use of a lux-modified bacterial biosensor to identify constraints to bioremediation of BTEX-contaminated sites. Environmental Toxicology and Chemistry, 17, 1039–45.
Steinberg, S. M., Poziomek, E. J., Engelmann, W. H. & Rogers, K. R. (1995). A review of environmental applications of bioluminescence measurements. Chemosphere, 30, 2155–97.
Strachan, G., Capel, S., Maciel, H., Porter, A. J. R. & Paton, G. I. (2002). Application of cellular and immunological biosensor techniques to assess herbicide toxicity in soils. European Journal of Soil Science, 53, 37–44.
Szittner, R., Jansen, G., Thomas, D. Y. & Meighen, E. (2003). Bright stable luminescent yeast using bacterial luciferase as a sensor. Biochemical and Biophysical Research Communications, 309, 66–70.
Tandy, S., Barbosa, V., Tye, A., Preston, S., Paton, G., Zhang, H. & McGrath, S. (2005). Comparison of different microbial bioassays to assess metal-contaminated soils. Environmental Toxicology and Chemistry, 24, 530–6.
Ulitzur, S. (1997). Established technologies and new approaches in applying luminous for analytical purposes. Journal of Bioluminescence and Chemiluminescence, 12, 179–92.
Vieites, J. M., Navarro-Garcia, F., Perez-Diaz, R., Pla, J. & Nombela, C. (1994). Expression and in vivo determination of firefly luciferase as gene reporter in Saccharomyces cerevisiae. Yeast, 10, 1321–7.
Walmsley, R. M. & Keenan, P. (2000). The eukaryote alternative: advantage of using yeasts in place of bacteria in microbial biosensor development. Biotechnology and Bioprocess Engineering, 5, 387–94.
Wassink, E. C. (1978). Luminescence in fungi. In Bioluminescence in Action, ed. Herring, P. J.. London: Academic Press, pp. 171–95.
Webb, J. S, Barratt, S. R., Sabev, H., Nixon, M., Eastwood, I. M., Greenhalgh, M., Handley, P. S. & Robson, G. D. (2001). Green fluorescent protein as a novel indicator of antimicrobial susceptibility in Aureobasidium pullulans. Applied and Environmental Microbiology, 67, 5614–20.
Weitz, H. J., Ritchie, J. M., Bailey, D. A., Horsburgh, A. M., Killham, K. & Glover, L. A. (2001a). Construction of a modified mini-Tn5 luxCDABE transposon for the development of bacterial biosensors for ecotoxicity testing. FEMS Microbiology Letters, 197, 159–65.
Weitz, H. J., Ballard, A. L., Campbell, C. D. & Killham, K. (2001b). The effect of culture conditions on the mycelial growth and luminescence of naturally bioluminescent fungi. FEMS Microbiology Letters, 202, 165–70.
Weitz, H. J., Campbell, C. D. & Killham, K. (2002). Development of a novel, bioluminescence-based, fungal bioassay for toxicity testing. Environmental Microbiology, 4, 422–9.
Wilson, T. & Hastings, J. W. (1998). Bioluminescence. Annual Review of Cell and Developmental Biology, 14, 197–230.