Highly efficient detoxification of dinitrotoluene by transgenic switchgrass overexpressing bacterial nitroreductase.
Biodegradation, Environmental
Catalysis
Dinitrobenzenes
/ metabolism
Enterobacter cloacae
/ enzymology
Gene Expression Profiling
Hydrogen-Ion Concentration
NADP
/ metabolism
Nitroreductases
/ metabolism
Panicum
/ enzymology
Plant Roots
/ growth & development
Plants, Genetically Modified
/ enzymology
Reactive Oxygen Species
/ metabolism
DNT
NfsI
phytoremediation
transgenic plants
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
received:
09
02
2021
accepted:
12
05
2021
pubmed:
20
5
2021
medline:
15
12
2021
entrez:
19
5
2021
Statut:
ppublish
Résumé
Dinitrotoluene (DNT) has been extensively used in manufacturing munitions, polyurethane foams and other important chemical products. However, it is highly toxic and mutagenic to most organisms. Here, we synthesized a codon-optimized bacterial nitroreductase gene, NfsI, for plant expression. The kinetic analysis indicates that the recombinant NfsI can detoxify both 2,4-DNT and its sulfonate (DNTS), while it has a 97.6-fold higher catalytic efficiency for 2,4-DNT than DNTS. Furthermore, we overexpressed NfsI in switchgrass (Panicum virgatum L.), which is a multiple-purpose crop used for fodder and biofuel production as well as phytoremediation. The 2,4-DNT treatment inhibited root elongation of wild-type switchgrass plants and promoted reactive oxygen species (ROS) accumulation in roots. In contrast, overexpression of NfsI in switchgrass significantly alleviated 2,4-DNT-induced root growth inhibition and ROS overproduction. Thus, the NfsI overexpressing transgenic switchgrass plant removed 94.1% 2,4-DNT after 6 days, whose efficiency was 1.7-fold higher than control plants. Moreover, the comparative transcriptome analysis suggests that 22.9% of differentially expressed genes induced by 2,4-DNT may participate in NfsI-mediated 2,4-DNT detoxification in switchgrass. Our work sheds light on the function of NfsI during DNT phytoremediation for the first time, revealing the application potential of switchgrass plants engineered with NfsI.
Substances chimiques
Dinitrobenzenes
0
Reactive Oxygen Species
0
NADP
53-59-8
Nitroreductases
EC 1.7.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3173-3183Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
Akkaya, Ö. (2020). Nicotiana tabacum-associated bioengineered Pseudomonas putida can enhance rhizoremediation of soil containing 2,4-dinitrotoluene. 3 Biotech, 10, 1-11.
Alexandrova, K. S., Denchev, P. D., & Conger, B. V. (1996). Micropropagation of switchgrass by node culture. Crop Science, 36, 1709-1711.
Brentner, L. B., Mukherji, S. T., Walsh, S. A., & Schnoor, J. L. (2010). Localization of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) and 2,4,6-trinitrotoluene (TNT) in poplar and switchgrass plants using phosphor imager autoradiography. Environmental Pollution, 158, 470-475.
Bryant, C., & DeLuca, M. (1991). Purification and characterization of an oxygen-insensitive NAD(P)H nitroreductase from Enterobacter cloacae. The Journal of Biological Chemistry, 266, 4119-4125.
Bryant, C., Hubbard, L., & McElroy, W. D. (1991). Cloning, nucleotide sequence, and expression of the nitroreductase gene from Enterobacter cloacae. The Journal of Biological Chemistry, 266, 26-33.
Chauviac, F. X., Bommer, M., Yan, J., Parkin, G., Daviter, T., Lowden, P., … Keep, N. H. (2012). Crystal structure of reduced MsAcg, a putative nitroreductase from Mycobacterium smegmatis and a close homologue of Mycobacterium tuberculosis Acg. The Journal of Biological Chemistry, 287, 44372-44383.
Doty, S. L. (2008). Enhancing phytoremediation through the use of transgenics and endophytes. The New Phytologist, 179, 318-333.
Ekman, D. R., Lorenz, W. W., Przybyla, A. E., Wolfe, N. L., & Dean, J. F. D. (2003). SAGE analysis of transcriptome responses in Arabidopsis roots exposed to 2,4,6-trinitrotoluene. Plant Physiology, 133, 1397-1406.
Gandia-Herrero, F., Lorenz, A., Larson, T., Graham, I. A., Bowles, D. J., Rylott, E. L., & Bruce, N. C. (2008). Detoxification of the explosive 2,4,6-trinitrotoluene in Arabidopsis: Discovery of bifunctional O- and C-glucosyltransferases. The Plant Journal, 56, 963-974.
Gilbert, E. E. (1977). Recovery of organic values from TNT purification waste water. Propellants, Explosives, Pyrotechnics, 2, 118-125.
Gong, P., Kuperman, R. G., & Sunahara, G. I. (2003). Genotoxicity of 2,4- and 2,6-dinitrotoluene as measured by the Tradescantia micronucleus (Trad-MCN) bioassay. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 538, 13-18.
Gunning, V., Tzafestas, K., Sparrow, H., Johnston, E. J., Brentnall, A. S., Potts, J. R., … Bruce, N. C. (2014). Arabidopsis glutathione transferases U24 and U25 exhibit a range of detoxification activities with the environmental pollutant and explosive 2,4,6-trinitrotoluene. Plant Physiology, 165, 854-865.
Hannink, N., Rosser, S. J., French, C. E., Basran, A., Murray, J. A. H., Nicklin, S., & Bruce, N. C. (2001). Phytodetoxification of TNT by transgenic plants expressing a bacterial nitroreductase. Nature Biotechnology, 19, 1168-1172.
Hardin, C. F., Fu, C., Hisano, H., Xiao, X., Shen, H., Stewart, C. N., … Wang, Z. Y. (2013). Standardization of switchgrass sample collection for cell wall and biomass trait analysis. Bioenergy Research, 6, 755-762.
Johnson, G. R., Jain, R. K., & Spain, J. C. (2002). Origins of the 2,4-dinitrotoluene pathway. Journal of Bacteriology, 184, 4219-4232.
Johnston, E. J., Rylott, E. L., Beynon, E., Lorenz, A., Chechik, V., & Bruce, N. C. (2015). Monodehydroascorbate reductase mediates TNT toxicity in plants. Science, 349, 1072-1075.
Kim, H. Y., & Song, H. G. (2005). Purification and characterization of NAD(P)H-dependent nitroreductase I from Klebsiella sp. C1 and enzymatic transformation of 2,4,6-trinitrotoluene. Applied Microbiology and Biotechnology, 68, 766-773.
Kist, C. P., Scherer, C. E., Soares, M., & Rodrigues, M. B. (2020). Biodegradation of nitroaromatic compounds in red water by white rot fungi pleurotus ostreatus and floridae. Revista Ambiente e Água, 15, e2594.
Koder, R. L., & Miller, A. F. (1998). Steady-state kinetic mechanism, stereospecificity, substrate and inhibitor specificity of Enterobacter cloacae nitroreductase. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, 1387, 395-405.
Kumar, D., Yusuf, M. A., Singh, P., Sardar, M., & Sarin, N. B. (2013). Modulation of antioxidant machinery in α-tocopherol-enriched transgenic Brassica juncea plants tolerant to abiotic stress conditions. Protoplasma, 250, 1079-1089.
Lent, E. M., Crouse, L. C. B., Quinn, M. J., & Wallace, S. M. (2012). Assessment of the in vivo genotoxicity of isomers of dinitrotoluene using the alkaline comet and peripheral blood micronucleus assays. Mutation Research-Genetic Toxicology and Environmental Mutagenesis, 742, 54-60.
Mann, D. G. J., King, Z. R., Liu, W., Joyce, B. L., Percifield, R. J., Hawkins, J. S., … Stewart, C. N. (2011). Switchgrass (Panicum virgatum L.) polyubiquitin gene (PvUbi1 and PvUbi2) promoters for use in plant transformation. BMC Biotechnology, 11.74
Mann, D. G. J., LaFayette, P. R., Abercrombie, L. L., King, Z. R., Mazarei, M., Halter, M. C., … Stewart, C. N. (2012). Gateway-compatible vectors for high-throughput gene functional analysis in switchgrass (Panicum virgatum L.) and other monocot species. Plant Biotechnology Journal, 10, 226-236.
Noctor, G., Mhamdi, A., & Foyer, C. H. (2016). Oxidative stress and antioxidative systems: Recipes for successful data collection and interpretation. Plant, Cell & Environment, 39(5), 1140-1160.
Puigbò, P., Guzmán, E., Romeu, A., & Garcia-Vallvé, S. (2007). OPTIMIZER: A web server for optimizing the codon usage of DNA sequences. Nucleic Acids Research, 35, W126-W131.
Rai, P. K., Kim, K. H., Lee, S. S., & Lee, J. H. (2020). Molecular mechanisms in phytoremediation of environmental contaminants and prospects of engineered transgenic plants/microbes. Scienceof theTotal Environment, 705, 135858.
Rao, M. R., Halfhill, M. D., Abercrombie, L. G., Ranjan, P., Abercrombie, J. M., Gouffon, J. S., … Stewart, C. N. (2009). Phytoremediation and phytosensing of chemical contaminants, RDX and TNT: Identification of the required target genes. Functional & Integrative Genomics, 9, 537-547.
Rich, M. H., Sharrock, A. V., Hall, K. R., Ackerley, D. F., & MacKichan, J. K. (2018). Evaluation of NfsA-like nitroreductases from Neisseria meningitidis and Bartonella henselae for enzyme-prodrug therapy, targeted cellular ablation, and dinitrotoluene bioremediation. Biotechnology Letters, 40, 359-367.
Rickert, D. E., Butterworth, B. E., Popp, J. A., & Krahn, D. F. (1984). Dinitrotoluene: Acute toxicity, oncogenicity, genotoxicity, and metabolism. Critical Reviews in Toxicology, 13, 217-234.
Roldán, M. D., Pérez-Reinado, E., Castillo, F., & Moreno-Vivián, C. (2008). Reduction of polynitroaromatic compounds: The bacterial nitroreductases. FEMS Microbiology, 32, 474-500.
Song, G., Yuan, S. X., Wen, X. H., Xie, Z. I., Lou, L. Q., Hu, B. Y., … Xu, B. (2018). Transcriptome analysis of cd-treated switchgrass root revealed novel transcripts and the importance of HSF/HSP network in switchgrass Cd tolerance. Plant Cell Reports, 37, 1485-1497.
Tognetti, V. B., Monti, M. R., Valle, E. M., Carrillo, N., & Smania, A. M. (2007). Detoxification of 2,4-dinitrotoluene by transgenic tobacco plants expressing a bacterial flavodoxin. Environmental Science & Technology, 41, 4071-4076.
Tsai, T. S. (1991). Biotreatment of red water-A hazardous-waste stream from explosive manufacture-With fungal systems. Hazardous Waste & Hazardous Materials, 8, 231-244.
Van Dillewijn, P., Couselo, J. L., Corredoira, E., Delgado, A., Wittich, R. M., Ballester, A., & Ramos, J. L. (2008). Bioremediation of 2,4,6-trinitrotoluene by bacterial nitroreductase expressing transgenic aspen. Environmental Science and Technology, 42, 7405-7410.
Williams, E.M., Sharrock, A. V, Rylott, E.L., Bruce, N.C., MacKichan, J.K., Ackerley, D.F., 2019. A cofactor consumption screen identifies promising NfsB family nitroreductases for dinitrotoluene remediation. Biotechnology Letters 41, 1155-1162.
Wise, A. A., Liu, Z., & Binns, A. N. (2006). Three methods for the introduction of foreign DNA into Agrobacterium. Methods in Molecular Biology, 343, 43-53.
Wu, Z. Y., Cao, Y. P., Yang, R. J., Qi, T. X., Hang, Y. Q., Lin, H., … Fu, C. X. (2016). Switchgrass SBP-box transcription factors PvSPL1 and 2 function redundantly to initiate side tillers and affect biomass yield of energy crop. Biotechnology for Biofuels, 9, 101.
Xiong, W. D., Wu, Z. Y., Liu, Y. C., Li, Y., Su, K. L., Bai, Z. T., … Fu, C. X. (2019). Mutation of 4-coumarate: Coenzyme a ligase 1 gene affects lignin biosynthesis and increases the cell wall digestibility in maize brown midrib5 mutants. Biotechnology for Biofuels, 12, 82.
Xu, W. J., Zhao, Q. L., Li, Z. L., Lu, X. Y., Han, S. Q., & Ye, Z. F. (2019). Biodegradation of dinitrotoluene sulfonates and other nitro-aromatic compounds by Pseudomonas sp. X5 isolated from TNT red water contaminated soil. Journal of Cleaner Production, 214, 782-790.
Zajc, B. (1999). Synthesis of (±)-trans-7,8-dihydrodiol of 6-fluoro-benzo[a]pyrene via hydroxyl-directed regioselective functionalization of substituted pyrene. The Journal of Organic Chemistry, 64, 1902-1907.
Zhang, L., Routsong, R., Nguyen, Q., Rylott, E. L., Bruce, N. C., & Strand, S. E. (2017a). Expression in grasses of multiple transgenes for degradation of munitions compounds on live-fire training ranges. Plant Biotechnology Journal, 15, 624-633.
Zhang, L., Rylott, E. L., Bruce, N. C., & Strand, S. E. (2017b). Phytodetoxification of TNT by transplastomic tobacco (Nicotiana tabacum) expressing a bacterial nitroreductase. Plant Molecular Biology, 95, 99-109.
Zhang, L., Rylott, E. L., Bruce, N. C., & Strand, S. E. (2019). Genetic modification of western wheatgrass (Pascopyrum smithii) for the phytoremediation of RDX and TNT. Planta, 249, 1007-1015.
Ziganshin, A. M., Naumov, A. V., Suvorova, E. S., Naumenko, E. A., & Naumova, R. P. (2007). Hydride-mediated reduction of 2,4,6-trinitrotoluene by yeasts as the way to its deep degradation. Microbiology, 76, 676-682.