Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-24T23:53:17.425Z Has data issue: false hasContentIssue false

Molecular Basis for Differential Metabolic Responses to Monosulfuron in Three Nitrogen-Fixing Cyanobacteria

Published online by Cambridge University Press:  20 January 2017

Jianying Shen*
Affiliation:
Dept. of Environmental Science and Resource, College of Agriculture and Life Science, Shanghai Jiaotong University, Shanghai, 200240, China
Antonio DiTommaso
Affiliation:
Dept. of Crop and Soil Sciences, Cornell University, Ithaca, NY 14853
Mingquan Shen
Affiliation:
Dept. of Environmental Science and Resource, College of Agriculture and Life Science, Shanghai Jiaotong University, Shanghai, 200240, China
Wei Lu
Affiliation:
Dept. of Environmental Science and Resource, College of Agriculture and Life Science, Shanghai Jiaotong University, Shanghai, 200240, China
Zhengming Li
Affiliation:
National Pesticide Engineering Research Center, Tianjin 300071, China
*
Corresponding author's E-mail: jyshen88@sjtu.edu.cn

Abstract

Nitrogen-fixing cyanobacteria are vital photosynthetic microorganisms that contribute to soil fertility by fixing atmospheric nitrogen and are also important for maintaining ecosystem stability. These microorganisms can be very sensitive to herbicides because they possess many characteristics of higher plants. Six days after the application of monosulfuron at 0.03 to 0.3 nmol L−1 under laboratory conditions, growth of the nitrogen-fixing cyanobacteria Anabaena flos-aquae, Anabaena azollae, and Anabaena azotica was stimulated, but at higher concentrations (30 to 300 nmol L−1) protein synthesis was inhibited. The production of 16 amino acids in A. flos-aquae was reduced from 7 to 69% with increasing monosulfuron concentration. Application of monosulfuron at 3 to 300 nmol L−1 substantially inhibited in vitro acetolactate synthase (ALS) activity as indicated by 50% inhibition index values of 3.3, 65.2, and 101.3 nmol L−1 for A. flos-aquae, A. azollae, and A. azotica, respectively. In contrast, extractable ALS activity was not affected in these algal species with monosulfuron treatments ranging from 0.03 to 300 nmol L1 except in A. flos-aquae at higher concentrations (30 to 300 nmol L−1). The most sensitive species to monosulfuron was A. flos-aquae, followed by A. azollae and A. azotica. Molecular analyses showed that the genomic DNA of A. azollae and A. azotica differed in only one amino acid. Results from photogenetic analyses revealed a high degree of homology between these algae. In contrast, the genomic DNA of A. flos-aquae differed from that of A. azollae and A. azotica in 44 and 45 amino acids, respectively. Our findings support the view that monosulfuron toxicity in these three nitrogen-fixing cyanobacteria is due to interference with protein metabolism via inhibition of branch-chain amino acid biosynthesis, and particularly ALS activity.

Type
Physiology, Chemistry, and Biochemistry
Copyright
Copyright © Weed Science Society of America 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Abou-Waly, H., Abou-Setta, M. M., Nigg, H. N., and Mallory, L. L. 1991. Growth response of freshwater algae, Anabaena flos-aquae and Selenastrum capricornutum, to atrazine and hexazinone herbicides. Bull. Environ. Contam. Toxicol. 46:223229.CrossRefGoogle ScholarPubMed
Barak, Z., Calvo, J. M., and Schloss, J. V. 1988. Acetolactate synthase isozyme III from Escherichia coli . Methods Enzymol. 166:455458.Google Scholar
Bhunia, A. K., Basu, N. K., Roy, D., Chakrabarti, A., and Banerjee, S. K. 1991. Growth, chlorophyll a content, nitrogen-fixing ability, and certain metabolic activities of Nostoc muscorum: effect of methylparathion and benthiocarb. Bull. Environ. Contam. Toxicol. 471:4350.Google Scholar
Blanck, H., Wallin, G., and Wangbery, S. 1984. Species-dependent variation in algal sensitivity to compounds. Ecotoxicol. Environ. Saf. 8:339351.Google Scholar
Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248254.Google Scholar
Bueno, M., Fillat, M. F., Strasser, R. J., Maldonado-Rodriguez, R., Marina, N., Smienk, H., Gomez-Moreno, C., and Barja, F. 2004. Effects of lindane on the photosynthetic apparatus of the cyanobacterium Anabaena: fluorescence induction studies and immunolocalization of ferredoxin-NADP+ reductase. Environ. Sci. Pollut. Res. Int. 11:98106.Google Scholar
Calabrese, E. J. 2005. Paradigm lost, paradigm found: the re-emergence of hormesis as a fundamental dose response model in the toxicological sciences. Environ. Pollut. 138:379412.Google Scholar
Calabrese, E. J. and Baldwin, L. A. 2003. Hormesis: the dose-response revolution. Ann. Rev. Pharmacol. Toxicol. 43:175–106.Google Scholar
Chaleff, R. S. and Mauvais, C. J. 1984. Acetolactate synthase is the site action of two sulfonylurea herbicides in higher plants. Science. 224:14431444.Google Scholar
Chen, J., Zheng, H. W., Shong, T. Y., Xi, G. Z., and Tong, L. F. 2001. The genetic diversity of Anabaena azollae based on RAPD analysis. Acta Hydrobiol. Sin. 25:531534.Google Scholar
Dastgheib, F. and Field, R. J. 1998. Acetolactate synthase activity and chlorsulfuron sensitivity of wheat cultivars. Weed Res. 38:6368.Google Scholar
Durner, J., Gailus, V., and Boger, P. 1991. New aspects on inhibition of plant acetolactate synthase by chlorsulfuron and imazaquin. Plant Physiol. 95:11441149.Google Scholar
El-Sheekh, M. M., Kotkat, H. M., and Hammouda, H. E. 1994. Atrazine herbicide on growth, photosynthesis, protein synthesis, and fatty acid composition in the unicellular green algae Chlorella kessler . Ecotoxicol. Environ. Saf. 29:349358.Google Scholar
Fan, Z. J., Ai, Y. W., Qian, C. F., and Li, Z. M. 2005. Herbicide activity of monosulfuron and its mode of action. J. Environ. Sci. (China) 17:399403.Google Scholar
Fan, Z. J., Hu, J. Y., Ai, Y. W., Qian, C. F., Yu, W. Q., and Li, Z. M. 2004. Residue analysis and dissipation of monosulfuron in soil and wheat. J. Environ. Sci. (China) 16:717721.Google Scholar
Fan, Z. J., Qian, C. F., and Dang, H. B. 2000. Study on the bioassay of maiguning and safety assessment of maiguning to different maize (Zea mays L.). Chin. J. Pestic. Sci. 2:6370.Google Scholar
Gruenhagen, R. D. and Moreland, D. E. 1971. Effects of herbicides on ATO levels in excised soybean hypocotyls. Weed Sci. 19:319323.Google Scholar
Guttieri, M. J., Eberlein, C. V., and Thill, D. C. 1995. Diverse mutations in the acetolactate synthase gene confer chlorsulfuron resistance in kochia (Kochia scoparia) biotypes. Weed Sci. 43:175178.CrossRefGoogle Scholar
Habte, M. and Alexander, M. 1980. Nitrogen fixation by photosynthetic bacteria in lowland rice culture. Appl. Environ. Microbiol. 39:342347.Google Scholar
Hirschberg, J. and Mclntosh, L. 1983. Molecular basis of herbicide resistance in Amaranthus hybridus . Science. 222:13461349.CrossRefGoogle ScholarPubMed
Hoare, D. S., Hoare, S. L., and Mcore, R. B. 1967. The photoassimilation of organic compounds by autotrophic blue-green algae. J. Gen. Microbiol. 49:351370.CrossRefGoogle Scholar
Irisarri, P., Gonnet, S., and Monza, J. 2001. Cyanobacteria in Uruguayan rice fields: diversity, nitrogen fixing ability and tolerance to herbicides and combined nitrogen. J. Biotechnol. 91:95103.CrossRefGoogle ScholarPubMed
Kamiya, A. and Kowallik, W. 1987. Photoinhibition of glucose uptake in Chlorella . Plant Cell Physiol. 28:611619.Google Scholar
Kaur, M., Ahluwalia, A. S., and Dahuja, S. 2002. Toxicity of a rice field herbicide in a nitrogen fixing alga, Cylindrospermum sp. J. Environ. Biol. 23:359363.Google Scholar
Koeppe, M. K., Hirata, C. M., and Brown, H. M. 2000. Basis of selectivity of the herbicide rimsulfuron in maize. Pestic. Biochem. Physiol. 66:170181.Google Scholar
Kratz, W. A. and Myers, J. 1955. Nutrition and growth of several blue-green algae. Am. J. Bot. 42:282287.Google Scholar
LaRossa, R. A. and Schloss, J. V. 1984. The sulfonylurea herbicide sulfometuron methyl is an extremely potent and selective inhibitor of acetolactate synthase in Salmonella typhimurium . J. Biol. Chem. 259:87538757.Google Scholar
LaRossa, R. A. and Van Dyk, T. K. 1988. Utilization of sulfometuron methyl, an acetolactate synthase inhibitor, in molecular biological and metabolic studies of plants and microbes. Methods Enzymol. 166:97107.Google Scholar
Leyval, D., Uy, D., Delaunay, S., Goergen, J. L., and Engasser, J. M. 2003. Characterization of the enzyme activities involved in the valine biosynthetic pathway in a valine-producing strain of Corynebacterium glutamicum . J. Biotechnol. 104:241252.Google Scholar
Li, S. H. 1962. Blue-green nitrogen-fixing cyanobacteria as fertilizer in rice fields. J. Hydrobiol. 1:5561.Google Scholar
Li, Z. M., Jia, G. F., and Wang, L. X. 1994. Sulfonylurea compounds and its herbicide usage. Chinese patent CNI 080 116A.Google Scholar
Milano, A., De Rossi, E., Zanaria, E., Barbierato, L., Ciferri, O., and Riccardi, G. 1992. Molecular characterization of the genes encoding acetohydroxy acid synthase in the cyanobacterium Spirulina platensis . J. Gen. Microbiol. 138:13991408.Google Scholar
Miquel, L. L. R. and Ivo, . 2006. On the way to cyanobacteria blooms: impact of the herbicide metribuzin on the competition between a green alga (Scenedesmus) and a cyanobacterium (Microcystis). Chemosphere. 65:618626.Google Scholar
Mishra, A. K. and Pandey, A. B. 1989. Toxicity of three herbicides to some nitrogen-fixing cyanobacteria. Ecotoxicol. Environ. Saf. 17:236246.Google Scholar
Pillmoor, J. B. 1989. Amino acid biosynthesis: an Aladdin's cave of new pesticide targets. Brighton Crop Prot. Conf. Mono. 42:2329.Google Scholar
Prithiviraj, B., Perry, L. G., Badri, D. V., and Vivanco, J. M. 2007. Chemical facilitation and induced pathogen resistance mediated by a root-secreted phytotoxin. New Phytol. 173:852860.CrossRefGoogle ScholarPubMed
Ray, T. 1984. Site of action of chlorsulfuron. Plant Physiol. 75:827831.Google Scholar
Saari, L. L., Cotterman, J. C., and Thill, D. C. 1994. Resistance to acetolactate synthase-inhibiting herbicides. Pages 83139. in Powles, S. B. and Holtum, J. A. M. Herbicide Resistance in Plants: Biology and Biochemistry. Ann Arbor, MI Lewis.Google Scholar
SAS Institute 2001. SAS/STAT Guide for personal computers, version 8.2. Cary, NC SAS Institute.Google Scholar
Schrader, K. K., Regt, M. Q., Tidwell, P. D., Tucker, C. S., and Duke, S. O. 1998. Compounds with selective toxicity towards the off-flavor metabolite-producing cyanobacterium Oscillatoria cf. chalybea . Aquaculture. 163:8591.Google Scholar
Shen, J. Y., Ding, H., She, Y., and Li, Z. M. 2008. Effects of monosulfuron and monosulfuron-ester on rice growth and efficacy control of weeds. Weed Sci. (China) 2:1317.Google Scholar
Shen, J. Y. and Lu, Y. 2005. Effects of herbicides on biodiversity of rice fields in China. Pages 5667. in. Proceedings of the Impact Assessment of Farm Chemicals Run-Off from Paddy Conference. Japan National Institute for Agro-Environmental Sciences, Japan (NIAES) and National Institute of Agricultural Science and Technology, Korea (NIAST).Google Scholar
Shen, J. Y., Lu, Y., and Cheng, G. 2005. Effects of chemical herbicides on toxicity of non-target nitrogen-fixing Cyanobacteria in paddy fields. Pages 665670. in. Proceedings of the 20th Asian-Pacific Weed Science Conference. Vietnam Weed Science Society Asian-Pacific.Google Scholar
Shen, J. Y., Lu, Z. R., Lu, Y. T., and Wang, X. H. 2004. Progress on toxicity of nitrogen-fixing cyanobacteria to herbicides. World Pestic. 6:5461.Google Scholar
Shen, L. W. and Li, S. H. 1993. Prospect and outcome in application and cultivation of blue-green nitrogen-fixing cyanobacteria. J. Hydrobiol. 17:357364.Google Scholar
Sibony, M. and Rubin, B. 2003. Molecular basis for multiple resistance to acetolactate synthase-inhibiting herbicides and atrazine in Amaranthus blitoides (prostrate pigweed). Planta. 216:10221027.Google Scholar
Sinha, R. P. and Kumar, A. 1992. Screening of blue-green algae for biofertlizer. Pages 9597. in. Proceedings of the National Seminar on Organic Farming (P. S. Patil, Ed.), Pune, India.Google Scholar
Tomilin, C. D. S. 2003. The Pesticide Manual. 13th ed. London The British Crop Protection Council. 1037.Google Scholar
Vyazmensky, M., Sella, C., Barak, Z., and Chipman, D. M. 1996. Isolation and characterization of subunits of acetohydroxyacid synthase isozyme III and reconstitution of the holoenzyme. Biochemistry. 35:1033910346.Google Scholar
Whitcomb, C. E. 1999. An introduction to ALS-inhibiting herbicides. Toxicol. Industr. Health. 15:232240.Google Scholar
Wu, X. Q., Zarka, A., and Boussiba, S. 2000. A simplified protocol for preparing DNA from filamentous cyanobacteria. Plant Mol. Biol. Rep. 18:385392.Google Scholar
Wu, Z. D. and Zhou, Y. Q. 2004. An introduction to Anabaena flos-aquae toxins. Yunnan Environ. Sci. 23:811.Google Scholar