Effect of a High Silver Stress on the Element Transfers from a Smectite-Type Clay Substrate to Plants

Khadija Semhi, Norbert Clauer, Sam Chaudhuri, René Boutin, Mohamed Hassan

Department of Geology, Kansas State University, Manhattan, USA.
Laboratoire d’Hydrologie et de Géochimie de Strasbourg (CNRS-UdS), Strasbourg, France.
Sultan Qaboos University, Muscat, Oman.

DOI: 10.4236/gsc.2012.22013                

Abstract

Two species of radishes, Raphanus sativus and Raphanus raphanistrum, were grown in the laboratory in the same substrate consisting of a smectite-type clay, which was watered at the beginning of the experience with 50 ml of a solution containing either none or 1000, 2000 or 4000 mg/L of AgNO3, respectively. Occurrence of the toxic metal in the substrate outlines higher element uptakes by the cultivated species Raphanus sativus than by the wild species Raphanus raphanistrum, except for the highest degree of Ag pollution. After a one-month growth in the Ag-polluted substrate, Raphanus sativus was depleted in most of the major, trace and rare-earth elements, except for Al, Fe, Th, Ag and U that increased in the radishes from substrate polluted by 2000 mg/L of AgNO3, and Sr, Co, Ni, U and Ag that increased in the radishes from substrate polluted by 4000 mg/L of AgNO3. Raphanus raphanistrum was enriched in all elements except Si, Na, Rb and K in the polluted substrate. The uptake was monitored by a cation-exchange process in the rhy-zosphere between mineral particles and the watering solution in the presence of various enzymes with specific activities that induced a variable uptake with the REEs being even fractionated. These activities most probably depend on combined factors, such as the plant species, and the chemical and physical properties of the substrate. The results obtained here reveal also that accumulation of nutrient elements and others in the plants is not uniform at a given Ag pollution of the substrate and therefore at a given Ag contamination in the same plant species.

Keywords

Ag Pollution; Plant-Growth Experiment; Smectite-Type Clay Substrate; Soil-Plant Element Transfers; REE Fractionation

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	T. W. Purcell and J. J. Peters, “Sources of Silver in the Environment: Silver Toxicity,” Environmental Toxico- logy and Chemistry, Vol. 17, No. 4, 1998, pp. 539-546.
[2]	K. E. Giller, E. Witter and S. P. McGrath, “Toxicity of Heavy Metals to Microorganisms and Microbial Processes in Agricultural Soils: A Review,” Soil Biology and Biochemistry, Vol. 30, No. 10-11, 1998, pp. 1389-1414. doi:10.1016/S0038-0717(97)00270-8
[3]	S. S. Sengor, S. Barua, P. Gikas, T. R. Ginn, B. Peyton, R. K. Sani and N. Spy-cher, “Influence of Heavy Metals on Microbial Growth Kinet-ics Including Lag Time: Mathe- matical Modelling and Experimental Verification,” Environmental Toxicology and Chemistry, Vol. 28, No. 10, 2009, pp. 2020-2029. doi:10.1897/08-273.1
[4]	M. Seif Sahandi, A. H. Soroosh-zadeh, S. Rezazadeh and H. A. Naghdibadi, “Effect of Nano Silver and Silver Nitrate on Seed Yield of Borage,” Journal of Medicinal Plants Research, Vol. 5, No. 2, 2011, pp. 171-175.
[5]	S. Silver and T. K. Misra, “Plasmid-Mediated Heavy Metal Resistances,” Annual Review in Microbiology, Vol. 42, 1988, pp. 717-743. doi:10.1146/annurev.mi.42.100188.003441
[6]	G. Tyler, P. A. M. Balsberg, G. Bengtsson, E. Baath and L. Tranvik, “Heavy-Metal Ecology of Terrestrial Plants, Microorganisms and Invertabrates,” Water, Air and Soil Pollution, Vol. 47, No. 3-4, 1989, pp. 189-215. doi:10.1007/BF00279327
[7]	C. Barnhart and J. R. Vestal, “Effects of Environmental Toxicants on Metabolic Activity of Natural Microbial Communities,” Applied Environmental Mi-crobiology, Vol. 46, No. 5, 1983, pp. 970-977.
[8]	W. A. Said and D. L. Lewis, “Quantitative Assessment of the Effects of Metals on Microbial Degradation of Organic Chemicals,” Applied Environmental Microbiology, Vol. 57, No. 5, 1991, pp. 1498-1503.
[9]	R.-A. Sandaa, ?. Enger and V. L. Torsvik, “Abundance and Diversity of Archaea in Heavy-Metal-Contaminated Soils,” Applied Environmental Microbiology, Vol. 65, No. 8, 1999, pp. 3293-3297.
[10]	S. I. Kolesnikov, K. S. Kazeev and V. F. Val’kov, “The Effect of Heavy Metal Contamination on the Microbial System in Chernozem,” Eurasian Soil Science, Vol. 32, No. 4, 1999, pp. 459-465.
[11]	H. N. P. John and R. S Tripathi, “Decomposition of Fine Roots of Pinus Kesiya and Turnover of Organic Matter, N and P of Course and Fine Pine Roots and Herbaceous Roots and Rhizomes in Subtropical Pine Forest Stands of Different Ages,” Biology Fertilizers and Soils, Vol. 35, No. 4, 2002, pp. 238-246. doi:10.1007/s00374-002-0470-8
[12]	F. Gremion, A. Chatzinotas, K. Kaufmann, W. Von Sigler and H. Harms, “Impacts of Heavy Metal Contamination and Phytoremediation on a Micro-bial Community during a Twelve-Month Microcosm Experiment,” FEMS Micro-biology Ecology, Vol. 48, No. 2, 2004, pp. 273-283. doi:10.1016/j.femsec.2004.02.004
[13]	C. Reimann and P. De Caritat, “Chemical Elements in the Environment. Facts Heets for the Geochemist and Environmental Scientist,” Springer Verlag, Heidelberg, 1998.
[14]	H. T. Ratte, “Bioaccumulation and Toxicity of Silver Compounds: A Review,” Environmental Toxicology and Chemistry, Vol. 18, No. 1, 1999, pp. 89-108. doi:10.1002/etc.5620180112
[15]	B. Isikili, T. A. Demir, ü. ?zelmas and A. Berber, “Effects of Silver on Humans Living Near a Silver Mine,” Journal of Medical Science, Vol. 28, No. 6, 1998, pp. 655-659.
[16]	M. C. Jung, “Heavy Metal Contamination of Soils and Waters in and Around the Imcheon Au-Ag Mine, Korea,” Applied Geochemistry, Vol. 16, No. 11-12, 2001, pp. 1369-1375. doi:10.1016/S0883-2927(01)00040-3
[17]	C. G. Lee, H.-T. Chon and M. C. Jung, “Heavy Metal Contamination in the Vi-cinity of the Daduk Au-Ag-Pb-Zn Mine in Korea,” Applied Geochemistry, Vol. 16, No. 11- 12, 2001, pp. 1377-1386. doi:10.1016/S0883-2927(01)00038-5
[18]	D. Cicchella, B. De Vivo, A. Lima, S. Albanese, R. A. R. McGill and R. R. Parrish, “Heavy Metal Pollution and Pb Isotopes in Urban Soils of Na-poli, Italy,” Geochemistry: Exploration, Environment, Analysis, Vol. 8, No. 1, 2008, pp. 103-112. doi:10.1144/1467-7873/07-148
[19]	A. H. Cornfield, “Effects of Addition of 12 Metals on Carbon Dioxide Release during Incubation of an Acid Sandy Soil,” Geoderma, Vol. 19, No. 3, 1977, pp. 199- 203. doi:10.1016/0016-7061(77)90027-1
[20]	T. Murata, M. Kanao-Koshikawa and T. Takamatsu, “Ef- fects of Pb, Cu, Sb, In and Ag Contamination on the Proliferation of Soil Bacterial Colonies, Soil Dehydrogenase Activity, and Phospholipid Fatty Acid Profiles of Soil Microbial Communities,” Water, Air and Soil Pollution, Vol. 164, No. 1-4, 2005, pp. 103-118. doi:10.1007/s11270-005-2254-x
[21]	T. Pümpel and F. Schinner, “Silver Tolerance and Silver Accumulation of Microor-ganisms from Oil Materials of a Silver Mine,” Applied Micro-biology and Biotechnology, Vol. 24, No. 3, 1986, pp. 244-247.
[22]	M. Johansson, M. Pell and J. Stenstrom, “Kinetics of Substrate-Induced Respiration (Sir) and Denitrification: Applications to a Soil Amended with Silver,” A Journal of the Human Environment, Vol. 27, No. 1, 1998, pp. 40- 44.
[23]	R. R. Brooks, M. F. Chambers, L. J. Nicks and B. H. Robinson, “Phytomining,” Trends in Plant Sciences, Vol. 3, No. 9, 1998, pp. 359-362. doi:10.1016/S1360-1385(98)01283-7
[24]	T. Andrew, A. E. Harris and R. Bali, “On the Formation and Extent of Uptake of Silver Nanoparticles by Live Plants,” Journal of Nanoparticle Research, Vol. 10, 4, 2008, pp. 691-695. doi:10.1007/s11051-007-9288-5
[25]	K. Semhi, N. Clauer and S. Chaudhuri, “Variable Element Transfers from an Illite-Rich Substrate to a Growing Plant during a Three-Month Experiment,” Applied Clay Science, Vol. 57, 2012, pp. 17-24. doi:10.1016/j.clay.2011.12.002
[26]	M. D. Moore and R. C. Reynolds Jr., “X-Ray Diffraction and the Identification and Analysis of Clay Minerals,” 2nd Edition, Oxford University Press, Oxford, 1997.
[27]	G. S. Odin and 35 Collaborators, “Interlaboratory Standards for Dating Purposes,” In: G. S. Odin, Ed., Numerical Dating in Stratigraphy, Part 1, John Wiley & Sons, Chichester, 1982, pp. 123-148.
[28]	K. Govin-daraju, “1994 Compilation of Working Values and Sample Description for 383 Geostandards,” Geo- standards Newsletter, Vol. 18, No. 1, 1994, pp. 1-158.
[29]	C. Y. Chiu, M. K. Wang, M. C. Chen and H. B. King, “Physical and Chemical Properties in Rhizosphere and Bulk Soils of Tsuga and Yushania in a Temperate Rain Forest,” Community Soil Science & Plant Analysis, Vol. 33, No. 11-12, 2002, pp. 1723-1735. doi:10.1081/CSS-120004818
[30]	J. F. Ma, “Plant Root Re-sponses to Three Abundant Soil Minerals: Silicon, Aluminum and Iron,” Critical Reviews in Plants, Vol. 24, No. 4, 2005, pp. 267-281. doi:10.1080/07352680500196017
[31]	S. Clemens, D. M. Antosiewicz, J. M. Ward, D. P. Schartman and J. I. Schroeder, “The Plant cDNA LCT1 Mediates the Uptake of Calcium and Cadmium in Yeast,” Plant Biology, Vol. 95, No. 20, 1998, pp. 12043-12048.
[32]	V. K. Harold and L. B. Karen, “Silver Up-take, Distribution, and Effect on Calcium, Phosphorus, and Sulfur Up-take,” Plant Physiology, Vol. 65, No. 2, 1980, pp. 336- 339. doi:10.1104/pp.65.2.336
[33]	P. P. Motavalli, R. J. Kremer, M. Fang and N. E. Means, “Impact of Genetically Modified Crops and Their Management on Soil Microbially Mediated Plant Nutrient Transformations,” Journal on Envi-ronmental Quality, Vol. 33, No. 3, 2004, pp. 816-824. doi:10.2134/jeq2004.0816
[34]	W. W. Barker, S. A Welch, S. Chu and J. F. Banfield, “Experimental Observations of the Effects of Bacteria on Aluminosilicate Weathering,” American Mineralogist, Vol. 83, No. 11-12, 1998, pp. 1551-1563.
[35]	K. Semhi, S. Chaudhuri and N. Clauer, “Fractionation of Rare-Earth Elements in Plants during an Experimental Growth in Varied Clay Substrates,” Applied Geochemis- try, Vol. 24, No. 3, 2009, pp. 447-453. doi:10.1016/j.apgeochem.2008.12.029
[36]	C. H. Evans, “Biochemistry of the Lanthanides,” Plenum Press, New York, 1990.
[37]	K. J. Cantrell and R. H. Byrne, “Rare Earth Element Complexation by Carbonate and Oxalate Ions,” Geochimica et Cosmochimica Acta, Vol. 51, No. 3, 1987, pp. 597-605. doi:10.1016/0016-7037(87)90072-X
[38]	F. J. Millero, “Sta-bility Constants for the Formation of Rare Earth Element Complexes as a Function of Ionic Strength,” Geochimica et Cosmo-chimica Acta, Vol. 56, No. 8, 1992, pp. 3123-3132. doi:10.1016/0016-7037(92)90293-R
[39]	L. Tao, D. Shiming, Z. Chaosheny, Z. Zili, Y. Juncai and L. Haitao, “Fractionation of Rare Earth Elements in Plant. I. Fractionation Patterns and Their Forming Mechanisms in Different Organs of Triticium aestivum,” Journal of Rare Earths, Vol. 23, 2005, pp. 224- 229.
[40]	A. Wyttenbach, V. Furrer, P. Schleppi and L. Tobler, “Rare Earth Elements in Soil and in Soil-Grown Plants,” Plant and Soil, Vol. 199, No. 2, 1998, pp. 267-273. doi:10.1023/A:1004331826160
[41]	F. F. Fu, T. Akage and K. Shinotsuka, “Distribution Patterns of Rare Earth Elements in Fern: Implication for In-take of Fresh Silicate Particles by Plants,” Biological Trace Element Research, Vol. 64, No. 1-3, 1998, pp. 13-26. doi:10.1007/BF02783321
[42]	Z. G. Wei, M. Yin and X. Zhang, “Rare Earth Elements in Naturally Grown Fern Dicranopteris linearis in Rela- tion to Their Variation in South-Jiangxi Region (Southern China),” Environmental Pollu-tion, Vol. 114, No. 3, 2001, pp. 345-355. doi:10.1016/S0269-7491(00)00240-2