Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-28T07:03:33.794Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of inorganic v. organic copper on denitrification in agricultural soil

Published online by Cambridge University Press:  27 September 2013

Q. Wang ,
M. Burger ,
T. A. Doane ,
W. R. Horwath ,
A. R. Castillo  and
F. M. Mitloehner
Q. Wang
Affiliation:
Department of Animal Science, University of California, Davis, 1 Shields Avenue, Davis, CA 95616, USA
M. Burger
Affiliation:
Department of Land, Air and Water Resources, University of California, Davis, 1 Shields Avenue, Davis, CA 95616, USA
T. A. Doane
Affiliation:
Department of Land, Air and Water Resources, University of California, Davis, 1 Shields Avenue, Davis, CA 95616, USA
W. R. Horwath
Affiliation:
Department of Land, Air and Water Resources, University of California, Davis, 1 Shields Avenue, Davis, CA 95616, USA
A. R. Castillo
Affiliation:
University of California Cooperative Extension Merced County, Merced, CA 95341, USA
F. M. Mitloehner*
Affiliation:
Department of Animal Science, University of California, Davis, 1 Shields Avenue, Davis, CA 95616, USA
*
†E-mail: fmmitloehner@ucdavis.edu
Get access

Abstract

Nitrous oxide reductase (N2OR), the enzyme responsible for the reduction of N2O to N2 in denitrification, uses copper (Cu) as its cofactor. Its activity is lowered under conditions of Cu deficiency. In general, high organic matter (OM) soil decreases Cu availability. The present study investigated different Cu forms, namely organic (ORG) v. inorganic (INO), and associated concentrations (750, 550, 125, 60 μg Cu/g soil) for their efficacy in affecting denitrification and especially N2OR activity in high OM peat soil in a water saturated anaerobic condition for 24 h. Gas and liquid samples were taken every 8 h and analyzed for NO3−, NO2−, N2O and N2. Inorganic Cu treatments did not affect N transformation rates and N2OR activity among the different treatments (P > 0.05) throughout the incubation compared with the control (CON). The ORG Cu treatments increased NO3− (P < 0.05), NO2− (P < 0.05) and N2O (P < 0.05) transformation rates compared with CON. These changes were ORG Cu dose dependent. N2OR activity increased first in the 750 μg ORG Cu treatment (P < 0.05) during 8 to 16 h followed by the other ORG Cu treatments (P < 0.05) during 16 to 24 h compared with CON. These results highlight the importance of Cu form and concentration on N transformation rate during denitrification. The findings can potentially be applied to systems like soil, wastewater, constructed wetlands, etc., in which reactions of the denitrification pathway are manipulated.

Keywords

inorganic copperorganic copperdenitrificationnitrous oxide reductase
Type
Full Paper
Information
Advances in Animal Biosciences , Volume 4 , Special Issue s1: Proceedings of the Dairy Solutions Symposium, 20th – 21st June 2012, University College Dublin, Dublin, Ireland , September 2013 , pp. 42 - 49
Copyright
Copyright © The Animal Consortium 2013 

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

Adriano, DC 2001. Trace elements in terrestrial environments: Biogeochemistry, bioavailability and risks of metals, 2nd edition. Springer, New York.CrossRefGoogle Scholar
Baggs, EM 2008. A review of stable isotope techniques for N2O source partitioning in soils: recent progress, remaining challenges and future considerations. Rapid Communications in Mass Spectrometry 22, 1664–1672.CrossRefGoogle ScholarPubMed
Betlach, MR, Tiedje, JM 1981. Kinetic explanation for accumulation of nitrite, nitric-oxide, and nitrous-oxide during bacterial denitrification. Applied and Environmental Microbiology 42, 1074–1084.CrossRefGoogle ScholarPubMed
Bleakley, BH, Tiedje, JM 1982. Nitrous-oxide production by organisms other than nitrifiers or denitrifiers. Applied and Environmental Microbiology 44, 1342–1348.CrossRefGoogle ScholarPubMed
Bolan, NS, Adriano, DC, Mahimairaja, S 2004. Distribution and bioavailability of trace elements in livestock and poultry manure by-products. Critical Reviews in Environmental Science and Technology 34, 291–338.CrossRefGoogle Scholar
Burgin, AJ, Hamilton, SK 2007. Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Frontiers in Ecology and the Environment 5, 89–96.CrossRefGoogle Scholar
Butler, CS, Fairhurst, SA, Ferguson, SJ, Thomson, AJ, Berks, BC, Richardson, DJ, Lowe, DJ 2002. Mo(V) co-ordination in the periplasmic nitrate reductase from Paracoccus pantotrophus probed by electron nuclear double resonance (ENDOR) spectroscopy. Biochemical Journal 363, 817–823.CrossRefGoogle ScholarPubMed
Cambillau, C, Brown, K, Djinovic-Carugo, K, Haltia, T, Cabrito, I, Saraste, M, Moura, JJG, Moura, I, Tegoni, M 2000. Revisiting the catalytic CuZ cluster of nitrous oxide (N2O) reductase – evidence of a bridging inorganic sulfur. Journal of Biological Chemistry 275, 41133–41136.Google Scholar
Carr, GJ, Ferguson, SJ 1990. The nitric-oxide reductase of paracoccus-denitrificans. Biochemical Journal 269, 423–429.CrossRefGoogle ScholarPubMed
CatalanSakairi, MA, Wang, PC, Matsumura, M 1997. High-rate seawater denitrification utilizing a macro-porous cellulose carrier. Journal of Fermentation and Bioengineering 83, 102–108.CrossRefGoogle Scholar
Cervantes, F, Monroy, O, Gomez, J 1998. Accumulation of intermediates in a denitrifying process at different copper and high nitrate concentrations. Biotechnology Letters 20, 959–961.CrossRefGoogle Scholar
Coyne, MS, Arunakumari, A, Averill, BA, Tiedje, JM 1989. Immunological identification and distribution of dissimilatory heme cd1 and nonheme copper nitrite reductases in denitrifying bacteria. Applied and Environmental Microbiology 55, 2924–2931.CrossRefGoogle ScholarPubMed
Doane, TA, Horwath, WR 2003. Spectrophotometric determination of nitrate with a single reagent. Analytical Letters 36, 2713–2722.CrossRefGoogle Scholar
Elliott, HA, Liberati, MR, Huang, CP 1986. Competitive adsorption of heavy-metals by soils. Journal of Environmental Quality 15, 214–219.CrossRefGoogle Scholar
Firestone, MK, Tiedje, JM 1979. Temporal change in nitrous-oxide and dinitrogen from denitrification following onset of anaerobiosis. Applied and Environmental Microbiology 38, 673–679.CrossRefGoogle ScholarPubMed
Gerzabek, MH, Lair, GJ, Haberhauer, G, Jakusch, M, Kirchmann, H 2006. Response of the sorption behavior of Cu, Cd, and Zn to different soil management. Journal of Plant Nutrition and Soil Science 169, 60–68.Google Scholar
Gigliotti, G, Businelli, D, Massaccesi, L, Said-Pullicino, D 2009. Long-term distribution, mobility and plant availability of compost-derived heavy metals in a landfill covering soil. Science of the Total Environment 407, 1426–1435.Google Scholar
Gilbert, FA 1952. Copper in nutrition. Advances in Agronomy 4, 147–177.CrossRefGoogle Scholar
Glass, C, Silverstein, J 1998. Denitrification kinetics of high nitrate concentration water: pH effect on inhibition and nitrite accumulation. Water Research 32, 831–839.CrossRefGoogle Scholar
Glockner, AB, Jungst, A, Zumft, WG 1993. Copper-containing nitrite reductase from Pseudomonas-Aureofaciens Is functional in a mutationally cytochrome-cd(1)-Free background (Nirs-) of Pseudomonas-Stutzeri. Archives of Microbiology 160, 18–26.CrossRefGoogle Scholar
Godden, JW, Turley, S, Teller, DC, Adman, ET, Liu, MY, Payne, WJ, Legall, J 1991. The 2.3 angstrom X-ray structure of nitrite reductase from Achromobacter-Cycloclastes. Science 253, 438–442.CrossRefGoogle ScholarPubMed
Granger, J, Ward, BB 2003. Accumulation of nitrogen oxides in copper-limited cultures of denitrifying bacteria. Limnology and Oceanography 48, 313–318.CrossRefGoogle Scholar
Haltia, T, Brown, K, Tegoni, M, Cambillau, C, Saraste, M, Mattila, K, Djinovic-Carugo, K 2003. Crystal structure of nitrous oxide reductase from Paracoccus denitrificans at 1.6 angstrom resolution. Biochemical Journal 369, 77–88.CrossRefGoogle Scholar
Hasnain, SS, Paraskevopoulos, K, Antonyuk, SV, Sawers, RG, Eady, RR 2006. Insight into catalysis of nitrous oxide reductase from high-resolution structures of resting and inhibitor-bound enzyme from Achromobacter cycloclastes. Journal of Molecular Biology 362, 55–65.Google Scholar
He, HB, Guan, TX, Zhang, XD, Bai, Z 2011. Cu fractions, mobility and bioavailability in soil-wheat system after Cu-enriched livestock manure applications. Chemosphere 82, 215–222.Google Scholar
Ho, TP, Jones, AM, Hollocher, TC 1993. Denitrification enzymes of Bacillus-Stearothermophilus. Fems Microbiology Letters 114, 135–138.CrossRefGoogle Scholar
Iwasaki, H, Terai, H 1982. Analysis of N2 and N2O produced during growth of denitrifying bacteria in copper-depleted and copper-supplemented media. Journal of General and Applied Microbiology 28, 189–193.CrossRefGoogle Scholar
Iwasaki, H, Saigo, T, Matsubara, T 1980. Copper as a controlling factor of anaerobic growth under N2O and biosynthesis of N2O reductase in denitrifying bacteria. Plant and Cell Physiology 21, 1573–1584.CrossRefGoogle ScholarPubMed
Jones, GB 1967. The movement of copper, molybdenum, and selenium in soils as indicated by radioactive isotopes. Australian Journal of Agricultural Research 18, 733–740.CrossRefGoogle Scholar
Knowles, R 1982. Denitrification. Microbiological Reviews 46, 43–70.CrossRefGoogle ScholarPubMed
Kornegay, ET, Hedges, JD, Martens, DC, Kramer, CY 1976. Effect on soil and plant mineral levels following application of manures of different copper contents. Plant and Soil 45, 151–162.CrossRefGoogle Scholar
Kroneck, PMH, Antholine, WA, Riester, J, Zumft, WG 1988. The cupric site in nitrous-oxide reductase contains a mixed-valence [Cu(Ii),Cu(I)] binuclear center – a multifrequency electron-paramagnetic resonance investigation. Febs Letters 242, 70–74.CrossRefGoogle Scholar
Kukimoto, M, Nishiyama, M, Murphy, MEP, Turley, S, Adman, ET, Horinouchi, S, Beppu, T 1994. X-ray structure and site-directed mutagenesis of a nitrite reductase from Alcaligenes-Faecalis S-6 – roles of 2 copper atoms in nitrite reduction. Biochemistry 33, 5246–5252.CrossRefGoogle Scholar
Kuper, J, Llamas, A, Hecht, HJ, Mendel, RR, Schwarz, G 2004. Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism. Nature 430, 803–806.CrossRefGoogle ScholarPubMed
Labbe, N, Parent, S, Villemur, R 2003. Addition of trace metals increases denitrification rate in closed marine systems. Water Research 37, 914–920.CrossRefGoogle ScholarPubMed
Lair, GJ, Gerzabek, MH, Haberhauer, G 2007. Sorption of heavy metals on organic and inorganic soil constituents. Environment Chemistry Letter 5, 23–27.CrossRefGoogle Scholar
LHerroux, L, LeRoux, S, Appriou, P, Martinez, J 1997. Behaviour of metals following intensive pig slurry applications to a natural field treatment process in Brittany (France). Environmental Pollution 97, 119–130.CrossRefGoogle ScholarPubMed
Libby, E, Averill, BA 1992. Evidence that the type-2 copper centers are the site of nitrite reduction by Achromobacter-Cycloclastes nitrite reductase. Biochemical and Biophysical Research Communications 187, 1529–1535.CrossRefGoogle ScholarPubMed
Lindsay, WL, Norvell, WA 1978. Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Science Society of America Journal 42, 421–428.CrossRefGoogle Scholar
Liu, MY, Liu, MC, Payne, WJ, Legall, J 1986. Properties and electron-transfer specificity of copper proteins from the denitrifier Achromobacter Cycloclastes. Journal of Bacteriology 166, 604–608.CrossRefGoogle ScholarPubMed
Lucas, RE 1948. Chemical and physical behavior of copper in organic soils. Soil Science 66, 119–129.CrossRefGoogle Scholar
Mathieu, O, Leveque, J, Henault, C, Milloux, MJ, Bizouard, F, Andreux, F 2006. Emissions and spatial variability of N2O, N2 and nitrous oxide mole fraction at the field scale, revealed with 15N isotopic techniques. Soil Biology & Biochemistry 38, 941–951.CrossRefGoogle Scholar
Matsubara, T, Frunzke, K, Zumft, WG 1982. Modulation by copper of theproducts of nitrite respiration in Pseudomonas-Perfectomarinus. Journal of Bacteriology 149, 816–823.CrossRefGoogle Scholar
Morrison, MS, Cobine, PA, Hegg, EL 2007. Probing the rold of copper in the biosynthesis of the molybdenum cofactor in Escherichia coli and Rhodobacter sphaeroides. Journal of Biological Inorganic Chemistry 12, 1129–1139.CrossRefGoogle Scholar
Oenema, O, Wrage, N, Velthof, GL, van Groenigen, JW, Dolfing, J, Kuikman, PJ 2005. Trends in global nitrous oxide emissions from animal production systems. Nutrient Cyclying in Agroecosystems 72, 51–65.CrossRefGoogle Scholar
Pathak, H 1999. Emissions of nitrous oxide from soil. Current Science 77, 359–369.Google Scholar
Paul, PP, Karlin, KD 1991. Functional-modeling of copper nitrite reductases- reactions of NO2 − or NO with copper(I) complexes. Journal of the American Chemical Society 113, 6331–6332.CrossRefGoogle Scholar
Richardson, D, Felgate, H, Watmough, N, Thomson, A, Baggs, E 2009. Mitigating release of the potent greenhouse gas N2O from the nitrogen cycle – could enzymic regulation hold the key? Trends in Biotechnology 27, 388–397.CrossRefGoogle ScholarPubMed
Scott, RA, Zumft, WG, Coyle, CL, Dooley, DM 1989. Pseudomonas-Stutzeri N2O reductase contains cua-type sites. Proceedings of the National Academy of Sciences of the United States of America 86, 4082–4086.CrossRefGoogle ScholarPubMed
Shapleigh, JP, Payne, WJ 1985. Differentiation of cd1 cytochrome and copper nitrite reductase production in denitrifiers. Fems Microbiology Letters 26, 275–279.Google Scholar
Stevens, RJ, Laughlin, RJ, Malone, JP 1998. Measuring the mole fraction and source of nitrous oxide in the field. Soil Biology & Biochemistry 30, 541–543.CrossRefGoogle Scholar
Stevenson, FJ 1994. Humus chemistry, 2nd edition. John Wiley & Sons Inc., New York.Google Scholar
Thomson, AJ, Rasmussen, T, Berks, BC, Butt, JN 2002. Multiple forms of the catalytic centre, Cu-z, in the enzyme nitrous oxide reductase from Paracoccus pantotrophus. Biochemical Journal 364, 807–815.Google Scholar
Thomson, AJ, Rasmussen, T, Berks, BC, Sanders-Loehr, J, Dooley, DM, Zumft, WG 2000. The catalytic center in nitrous oxide reductase, Cu-z, is a copper-sulfide cluster. Biochemistry 39, 12753–12756.Google Scholar
Verdouw, H, Vanechteld, CJA, Dekkers, EMJ 1978. Ammonia determination based on indophenol formation with sodium salicylate. Water Research 12, 399–402.CrossRefGoogle Scholar
Viebrock, A, Zumft, WG 1988. Molecular-cloning, heterologous expression, and primary structure of the structural gene for the copper enzyme nitrous-oxide reductase from denitrifying Pseudomonas-Stutzeri. Journal of Bacteriology 170, 4658–4668.CrossRefGoogle ScholarPubMed
Williams, DR, Rowe, JJ, Romero, P, Eagon, RG 1978. Denitrifying Pseudomonas-Aeruginosa – some parameters of growth and active-transport. Applied and Environmental Microbiology 36, 257–263.CrossRefGoogle ScholarPubMed