Abstract
Phytoremediation of highly water soluble and volatile organic xenobiotics is often inefficient because plants do not completely degrade these compounds through their rhizospheres. This results in phytotoxicity and/or volatilization of chemicals through the leaves, which can cause additional environmental problems. We demonstrate that endophytic bacteria equipped with the appropriate degradation pathway improve the in planta degradation of toluene. We introduced the pTOM toluene-degradation plasmid of Burkholderia cepacia G4 into B. cepacia L.S.2.4, a natural endophyte of yellow lupine. After surface-sterilized lupine seeds were successfully inoculated with the recombinant strain, the engineered endophytic bacteria strongly degraded toluene, resulting in a marked decrease in its phytotoxicity, and a 50–70% reduction of its evapotranspiration through the leaves. This strategy promises to improve the efficiency of phytoremediating volatile organic contaminants.
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References
Schnoor, L.J., Licht, A.L., McCutchon, C.S., Wolfe, N.L. & Carreira, H.L. Phytoremediation of organic and nutrient contaminants. Environ. Sci. Technol. 29, 318A–323A (1995).
Harvey P.J. et al. Phytoremediation of polyaromatic hydrocarbons, anilines and phenols. Environ. Sci. Pollut. Res. Int. 9, 29–47 (2002).
Cunningham, S.D. & Berti, W.B. Remediation of contaminated soils with green plants: an overview. In Vitro Cell. Dev. Biol. 29, 207–212 (1993).
Trapp, S., Köhler, A., Larsen, L.C., Zambrano, K.C. & Karlson, U. Phytotoxicity of fresh and weathered diesel and gasoline to willow and poplar trees. J. Soils Sed. 1, 71–76 (2001).
Trapp, S., Zambrano, K.C., Kusk, K.O. & Karlson, U. A phytotoxicity test using transpiration of willows. Arch. Environ. Contam. Toxicol. 39, 154–160 (2000).
Doucete, W.J. et al. Phytoremediation of dissolved phase trichloroethylene using mature vegetation. in Bioremediation and Phytoremediation: Chlorinated and Recalcitrant Compounds (eds. Wickraamanayakee, G.B. & Hinchee, R.E.) 251–256 (Battelle Press, Columbus, Ohio, USA, 1998).
Van der Lelie, D., Schwitzguebel, J.-P., Glass, D.J., Vangronsveld, J. & Baker A. Assessing phytoremediation's progress in the United States and Europe. Environ. Sci. Technol. 35, 446A–452A (2001).
Schwitzguebel, J.-P., van der Lelie, D., Glass, D.J., Vangronsveld, J. & Baker A. Phytoremediation: European and American trends, successes, obstacles and needs. J. Soil Sed. 2, 91–99 (2002).
Ma, X. & Burken, J.G. TCE diffusion to the atmosphere in phytoremediation applications. Environ. Sci. Technol. 37, 2534–2539 (2003).
Burken, J.G. & Schnoor, J.L. Distribution and volatilization of organic compounds following uptake by hybrid poplar trees. Int. J. Phytorem. 1, 139–151 (1999).
Misaghi, I.J. & Donndelinger, C.R. Endophytic bacteria in symptom free cotton plants. Phytopathol. 80, 808–811 (1990).
James, K. & Olivares, F.L. Infection and colonization of sugar cane and other Graminaceous plants by endophytic diazotrophs. Crit. Rev. Plant Sci. 17, 77–119 (1997).
Lodewyckx, C. et al. Endophytic bacteria and their potential applications. Crit. Rev. Plant Sci. 21, 583–606 (2002).
Frommel, M.I., Nowak, J. & Lazarovits, G. Growth enhancement and developmental modifications of in vitro grown potato (Solanum tuberosum ssp. Tuberosum) as affected by a nonfluorescent Pseudomonas sp. Plant Physiol. 96, 928–936 (1991).
Lodewyckx, C. et al. The effect of recombinant heavy metal resistant endophytic bacteria in heavy metal uptake by their host plant. Int. J. Phytorem. 3, 173–187 (2001).
Taghavi, S., Delanghe, H., Lodewyckx, C., Mergeay, M. & van der Lelie, D. Nickel-resistance-based minitransposons: new tools for genetic manipulation of environmental bacteria. Appl. Environ. Microbiol. 67, 1015–1019 (2001).
Reiter, B., Burgmann, H., Burg, K. & Sessitsch, A. Endophytic nifH gene diversity in African sweet potato. Can. J. Microbiol. 49, 549–555 (2003).
Bent, E. & Chanway, C.P. Potential for misidentification of a spore-forming Paenibacillus polymyxa isolate as an endophyte by using culture-based methods. Appl. Environ. Microbiol. 68, 4650–4652 (2002).
Elvira-Recuenco, M. & van Vuurde, J.W. Natural incidence of endophytic bacteria in pea cultivars under field conditions. Can. J. Microbiol. 46, 1036–1041 (2000).
Heyrman, J. et al. Bacillus novalis sp. nov., Bacillus vireti sp. nov., Bacillus soli sp. nov., Bacillus bataviensis sp. nov. and Bacillus drentensis sp. nov., from the Drentse A grasslands. Int. J. Syst. Evol. Microbiol. 54 (Pt 1), 47–57 (2004).
Siciliano, S.D. et al. Selection of specific endophytic bacterial genotypes by plants in response to soil contamination. Appl. Environ. Microbiol. 67, 2469–2475 (2001).
Sharp R.R., Bryers J.D., Jones W.G. & Shields, M.S. Activity and stability of a recombinant plasmid–borne TCE degradative pathway in suspended cultures. Biotechnol. Bioeng. 57, 287–296 (1998).
Shields, M.S. & Reagin, M.J. Selection of a Pseudomonas cepacia strain constitutive for the degradation of trichloroethylene. Appl. Environ. Microbiol. 58, 3977–3983 (1992).
Germaine, K. et al. Colonization of poplar trees by gfp expressing bacterial endophytes. FEMS Microbiol. Ecol. in the press (2004).
McCrady, J., Mc Farlane, C. & Lindstrom, F. The transport and affinity of substituted benzenes in soybean stems. J. Exp. Botany 38, 1875–1890 (1987).
Shields, M.S., Reagin, M.J., Gerger, R.R., Campbell, R. & Somerville, C. TOM, a new aromatic degradative plasmid from Burkolderia (Pseudomonas) cepacia G4. Appl. Environ. Microbiol. 61, 1352–1356 (1995).
Schlegel, H.G., Kaltwasser, H. & Gottschalk, G. Ein Sumbersverfahren zur Kultur wasserstoffoxidierender Bacterien: Wachstum physiologische Untersuchungen. Arch. Mikrobiol. 38, 205–222 (1961).
Mergeay, M., Nies, D., Schlegel, H.G., Gerits, J. & Van Gijsegem, F. Alcaligens eutrophus CH34 is a facultative chemolithotroph with plasmid–bound resistance to heavy metals. J. Bacteriol. 162, 328–334 (1985).
Acknowledgements
The European Commission under the Fifth Framework Program, Quality of Life supported this work by grant no. QLK3-2000-00164 entitled “Endegrade.” The work was also supported by Ford Motor Company (Genk Plant and the Environmental Quality Office Europe), which also provides experimental sites. We thank K. Germaine and E. Keogh for providing us with tomA specific primers, F. Tibaldi for statistic analysis of our data, D. Van Genechten for assisting in the conjugation experiments and J. Czech and R. Carleer for help with toluene analysis. Special thanks are due to M. Mergeay who interested us in the potential of endophytic bacteria. D.v.d.L. and S.T. are presently being supported by Laboratory Directed Research and Development funds at the Brookhaven National Laboratory under contract with the US Department of Energy. This paper is dedicated to the memory of Licy Oeyen.
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Barac, T., Taghavi, S., Borremans, B. et al. Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22, 583–588 (2004). https://doi.org/10.1038/nbt960
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DOI: https://doi.org/10.1038/nbt960
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