Plant Soil Environ., 2010, 56(8):357-367 | DOI: 10.17221/67/2010-PSE

Biogeochemical cycles of chlorine in the coniferous forest ecosystem: practical implications

M. Matucha1, N. Clarke2, Z. Lachmanová3, S.T. Forczek1, K. Fuksová4, M. Gryndler5
1 Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Prague, Czech Republic
2 Norwegian Forest and Landscape Institute, Aas, Norway
3 Forestry and Game Management Research Institute, Prague, Czech Republic
4 First Faculty of Medicine, Charles University, Prague, Czech Republic
5 Institute of Microbiology, Academy of Sciences of the Czech Republic, Prague, Czech Republic

Chlorine - one of the most widespread elements on the Earth - is present in the environment as chloride ion or bound to organic substances. The main source of chloride ions is the oceans while organically bound chlorine (OCl) comes from various sources, including anthropogenic ones. Chlorinated organic compounds were long considered to be only industrial products; nevertheless, organochlorines occur plentifully in natural ecosystems. However, recent investigations in temperate and boreal forest ecosystems have shown them to be products of biodegradation of soil organic matter under participation of chlorine. It is important to understand both the inorganic and organic biogeochemical cycling of chlorine in order to understand processes in the forest ecosystem and dangers as a result of human activities, i.e. emission and deposition of anthropogenic chlorinated compounds as well as those from natural processes. The minireview presented below provides a survey of contemporary knowledge of the state of the art and a basis for investigations of formation and degradation of organochlorines and monitoring of chloride and organochlorines in forest ecosystems, which has not been carried out in the Czech Republic yet.

Keywords: chlorine cycle; chlorination; enzymatic; abiotic; organochlorines; adsorbable organic halogenes

Published: August 31, 2010  Show citation

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Matucha M, Clarke N, Lachmanová Z, Forczek ST, Fuksová K, Gryndler M. Biogeochemical cycles of chlorine in the coniferous forest ecosystem: practical implications. Plant Soil Environ. 2010;56(8):357-367. doi: 10.17221/67/2010-PSE.
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References

  1. Adams J.M., Piovesan G. (2005): Long series relationships between global interannual CO 2 increment and climate: evidence for stability and change in role of the tropical and boreal-temperate zones. Chemosphere, 59: 1595-1612. Go to original source... Go to PubMed...
  2. Aamlid D., Horntvedt R. (2002): Sea salt impact on forests in western Norway. Forestry, 75: 171-178. Go to original source...
  3. Asplund G., Grimvall A., Pettersson C. (1989): Naturally produced organic halogens (AOX) in humic substances from soil and water. Science of the Total Environment, 81/82: 239-248. Go to original source...
  4. Asplund G., Grimvall A. (1991): Organohalogens in nature, more widespread than previously assumed. Environmental Science and Technology, 25: 1346-1350. Go to original source...
  5. Asplund G., Christiansen J.V., Grimvall A. (1993b): A chloroperoxidase-like catalyst in soil: detection and characterisation of some properties. Soil Biology and Biochemistry, 25: 41-46. Go to original source...
  6. Asplund G. (1995): Origin and occurrence of halogenated organic matter in soil. In: Grimvall A., de Leer E.W.B. (eds.): Naturally-Produced Organohalogens. Kluwer Academic Publishing, Dondrecht, 35-48. Go to original source...
  7. Bastviken D., Thompsen F., Karlsson S., Svensson T., Sandén P., Shaw G., Matucha M., Öberg G. (2007): Chloride retention in forest soil by microbial uptake and by natural formation of organochlorines. Geochimica et Cosmochimica Acta, 71: 3182-3192. Go to original source...
  8. Biester H., Keppler F., Putchew A., Martinez-Cortizas A., Petri M. (2004): Halogen retention, organohalogens, and the role of organic matter decomposition in two chilean peat bogs. Environmental Science and Technology, 38: 1984-1991. Go to original source... Go to PubMed...
  9. Christman R.F., Norwood D.L., Millington D.S., Johnson J.D. (1983): Identity and yields of major halogenated products of aquatic fulvic acid chlorination. Environmental Science and Technology, 17: 625-628. Go to original source... Go to PubMed...
  10. Clarke N., Fuksová K., Gryndler M., Lachmanová Z., Liste H.H., Rohlenová J., Schroll R., Schröder P., Matucha M. (2009): The formation and fate of chlorinated organic substances in temperate and boreal forest soils. Environmental Science and Pollution Research, 16: 127-143. Go to original source... Go to PubMed...
  11. de Leer W.B., Sinninghe Samete J.S., Erkelens C., de Galan L. (1985): Identification of intermediates leading to chloroform and C-4 diacids in the chlorination of humic acids. Environmental Science and Technology, 19: 512-522. Go to original source... Go to PubMed...
  12. de Jong E., Field J.A. (1997): Sulfur tuft and turkey tail: biosynthesis and biodegradation of organohalogenes by Basidiomycetes. Annual Review of Microbiology, 51: 375-414. Go to original source... Go to PubMed...
  13. Eriksson K.E., Blanchette R.A., Ander P. (1990): Microbial and Enzymatic Degradation of Wood and Wood Components, Springer-Verlag, Berlin, Heidelberg, 407. Go to original source...
  14. Fahimi I.J., Keppler F., Schöler H.F. (2003): Formation of chloroacetic acids from soil, humic acid and phenolic substances. Chemosphere, 52: 513-520. Go to original source... Go to PubMed...
  15. Flodin C., Johansson E., Borén H., Grimvall A., Dahlman O., Mörck R. (1997): Chlorinated structures in high molecular weight organic matter isolated from fresh and decaying plant material and soil. Environmental Science and Technology, 31: 2464-2468. Go to original source...
  16. Forczek S.T., Matucha M., Uhlířová H., Albrechtová J., Fuksová K., Schröder P. (2001): Biodegradation of trichloroacetic acid in Norway spruce/soil system. Biologia Plantarum, 44: 317-320. Go to original source...
  17. Forczek S.T., Schröder P., Weissflog L., Rohlenová J., Krüger G., Matucha M. (2007): Trichloroacetic acid of different origin in Norway spruce needles and chloroplasts. Biologia Plantarum, 52: 177-180. Go to original source...
  18. Fostad O., Pedersen P.O. (2000): Container grown tree seedlings responses to sodium chloride applications in different substrates. Environmental Pollution, 109: 203-210. Go to original source... Go to PubMed...
  19. Frank H., Scholl H., Renschen D., Rether D., Laouedj A., Norokorpi Y. (1994): Haloacetic acids, phytotoxic secondary air pollutants. Environmental Science and Pollution Research, 1: 4-14. Go to original source... Go to PubMed...
  20. Gage R.S., Aronoff S. (1960): Translocation III. experiments with carbon 14, chlorine 36, and hydrogen 3. Plant Physiology, 35: 53-64. Go to original source... Go to PubMed...
  21. Graedel T.E., Keene W.C. (1996): The budget and cycle of Earth's Natural chlorine. Pure and Applied Chemistry, 68: 1689-1697. Go to original source...
  22. Greenway H., Munns R. (1980): Mechanisms of salt tolerance in non-halophytes. Annual Review of Plant Physiology and Plant Molecular Biology, 31: 149-190. Go to original source...
  23. Gribble G.W. (2003): The diversity of naturally produced organohalogens. Chemosphere, 52: 289-298. Go to original source... Go to PubMed...
  24. Grinhut T., Hadar Y., Chen Y. (2007): Degradation and transformation of humic substances by saprotropic fungi: processes and mechanisms. Fungal Biology Reviews, 21: 179-189. Go to original source...
  25. Gryndler M., Rohlenová J., Kopecký J., Matucha M. (2 8): Chloride concentration affects soil microbial community. Chemosphere, 71: 1401-1408. Go to original source... Go to PubMed...
  26. Haiber G., Jacob G., Niedan V., Nkusi G., Schöler H.F. (1996): The occurrence of Trichloroacetic acid (TCAA) - indication of natural production? Chemosphere, 33: 839-849. Go to original source...
  27. Hamilton J.T.G., McRoberts W.C., Keppler F., Kalin R.M., Harper D.B. (2003): Chloride methylation by plant pectin: an efficient environmentally significant process. Science, 301: 206-208. Go to original source... Go to PubMed...
  28. Harper D.B. (1985): Halomethane from halide ion - a highly efficient fungal conversion of environmental significance. Nature, 315: 55-57. Go to original source...
  29. Hjelm O., Johansson M.B., Asplund-Öberg G. (1995): Organically bound halogens in Coniferous forest soil. Chemosphere, 30: 2353-2364. Go to original source...
  30. Hjelm O., Borén H., Öberg G. (1996): Analysis of halogenated organic compounds in Coniferous forest soil from a Lepista Nuda (Wood Blewitt) fairy ring. Chemosphere, 32: 1719-1728. Go to original source...
  31. Hjelm O., Johansson M.B., Öberg G. (1999): Production of organically bound halogens by the liter-degrading fungus Legista nuda. Soil Biology and Biochemistry, 31: 1509-1515. Go to original source...
  32. Hoekstra E.J., Verhagen F.J.M., Field J.A., de Leer E.W.B., Brinkman U.A.T. (1998): Natural production of chloroform by fungi. Phytochemistry, 49: 91-97. Go to original source...
  33. Hoekstra E.J., de Leer E.W.B., Brinkman U.A.Th. (1999a): Mass balance of trichloroacetic acid in the soil top layer. Chemosphere, 38: 551-563. Go to original source... Go to PubMed...
  34. Hoekstra E.J., de Leer E.W.B., Brinkman U.A.Th. (1999b): Findings supporting the natural formation of trichloroacetic acid in soil. Chemosphere, 38: 2875-2883. Go to original source...
  35. Hoekstra E.J., Duyzer J.H., de Leer E.W.B., Brinkman U.A.T. (2001): Chloroform-concentration gradients in soilair and atmospheric air, and emission fluxes from soil. Atmospheric Environment, 35: 61-70. Go to original source...
  36. Holst P.B., Christophersen C., Engvild K.C. (2000): In vivo incorporation of radioactive 36 Cl, a method for monitoring chloro compounds in biological material. Journal of Chromatography A, 903: 267-270. Go to original source... Go to PubMed...
  37. Huang L., Sturchio N.C., Abrajano T.Jr., Heraty L.J., Holt B.D. (1999): Carbon and chlorine fractionation of chlorinated aliphatic hydrocarbons by evaporation. Organic Geochemistry, 30: 777-785. Go to original source...
  38. Holmstrand H., Mandalakis M., Zencak Z., Gustafsson Ö., Andersson P. (2006): Chlorine isotope fractionation of a semi-volatile organochlorine compound during preparative megabore-column capillary gas chromatogramy. Journal of Chromatography A, 1103: 133-138. Go to original source... Go to PubMed...
  39. Johansson E., Krantz-Rülcker C., Zhang B.X., Öberg G. (2000): Chlorination and biodegradation of lignin. Soil Biology and Biochemistry, 32: 1029-1032. Go to original source...
  40. Johansson E., Sandén P., Öberg G. (2003): Organic chlorine in deciduous and coniferous forest soils in southern Sweden. Soil Science, 168: 347-355. Go to original source...
  41. Jones K.L., O´Melia CH.R. (2001): Ultrafiltration of protein and flux decline. Journal of Membrane Science, 193: 163-173. Go to original source...
  42. Kalbitz K., Schwesig D., Schmerwitz J., Kaiser K., Haumaier L., Laser B., Ellerbrock R., Leinweber P. (2003): Changes in properties of soil-derived dissolved organic matter induced by biodegradation. Soil Biology and Biochemistry, 35: 1129-1142. Go to original source...
  43. Kalbitz K., Solinger S., Park J.H., Michalzik B., Matzner E. (2000): Controls on the dynamics of dissolved organic matter in soils: a review. Soil Science, 165: 277-304. Go to original source...
  44. Keppler F., Eiden R., Niedan V., Pracht J., Schöler H.F. (2000): Halocarbons produced by natural oxidation processes during degradation of organic matter. Nature, 403: 298-301. Go to original source... Go to PubMed...
  45. Kozlowski T. (1997): Responses of Woody Plants to Flooding and Salinity. Tree Physiology Monograph 1. Heron Publishing, Victoria, 1-29. Go to original source...
  46. Krull E., Baldock J.A., Skjemstad J.O. (2003): Importance of mechanisms and processes of the stabilization of soil organic matter for modelling carbon turnover. Functional Plant Biology, 30: 207-222. Go to original source... Go to PubMed...
  47. Laturnus F., Mehrtens G., Groen C. (1995): Haloperoxidase-like activity in spruce forest soil- a source of volatile halogenated organic compounds? Chemosphere, 31: 3709-3719. Go to original source...
  48. Laturnus F., Haselmann K.F., Borch T., Grøn C. (2002): Terrestrial natural sources of trichloromethane (chloroform, CHCl3) - an overview. Biogeochemistry, 60: 121-139. Go to original source...
  49. Laturnus F., Fahimi I., Gryndler M., Hartman A., Heal M.R., Matucha M., Schöler H.F., Schroll R., Svenson T. (2005): Natural formation and degradation of chloroacetic acids and volatile organochlorine compounds in forest soil - challenges to understanding. Environ mental Science and Pollution Research, 12: 233-244. Go to original source... Go to PubMed...
  50. Laturnus F., Matucha M. (2008): Chloride - a pre-cursor in the formation of VOCls by forest plants? Journal of Environmental Radioactivity, 99: 119-125. Go to original source... Go to PubMed...
  51. Leri A.C., Hay M.B., Lanzirotti A., Rao W., Myneni S.C.B. (2006): Quantitative determination of absolute organohalogen concentrations in environmental samples by X-ray absorption spectroscopy. Analytical Chemistry, 78: 5711-5718. Go to original source... Go to PubMed...
  52. Leri A.C., Marcus M.A., Myneni S.C.B. (2007): X-ray spectromicroscopic investigation of natural organochlorine distribution in weathering plant material. Geochimica et Cosmochimica Acta, 71: 5834-5846. Go to original source...
  53. Lee R.T., Shaw G., Wadey P., Wang X. (2001): Specific association of 36 Cl with low molecular weight humic substances in soils. Chemosphere, 43: 1063-1070. Go to original source... Go to PubMed...
  54. Lin Ch.F., Huang Y.J., Hao O.J. (1999): Ultrafiltration processes for removing humic substances: effect of molecular weight fractions and PAC treatment. Water Research, 33: 1252-1264. Go to original source...
  55. Marschner B., Kalbitz K. (2003): Controls of bioavailability and biodegradability of dissolved organic matter in soils. Geoderma, 113: 211-235. Go to original source...
  56. Matucha M., Uhlířová H., Bubner M. (2001): Investigation of uptake, translocation and fate of trichloroacetic acid in Norway spruce. Chemosphere, 44: 217-222. Go to original source... Go to PubMed...
  57. Matucha M., Forczek S.T., Gryndler M., Uhlířová H., Fuksová K., Schröder P. (2003a): Trichloroacetic acid in Norway spruce/soilsystem. I. Biodegradation in soil. Chemosphere, 50: 303-309. Go to original source... Go to PubMed...
  58. Matucha M., Gryndler M., Forczek S.T., Uhlířová H., Fuksová K., Schröder P. (2003b): Chloroacetic acids in environmental processes. Environmental Chemistry Letters, 1: 127-130. Go to original source...
  59. Matucha M., Gryndler M., Uhlířová H., Fuksová K., Rohlenová J., Forczek S.T., Schröder P. (2004): Microbiological aspects of determination of trichloroacetic acid in soil. Folia Microbiologica, 49: 117-122. Go to original source... Go to PubMed...
  60. Matucha M., Rohlenová J., Forczek S.T., Uhlířová H., Gryndler M., Fuksová K., Schröder P. (2006): Determination of trichloroacetic acid in environmental studies using carbon 14 and chlorine 36. Chemosphere, 63: 1924-1932. Go to original source... Go to PubMed...
  61. Matucha M., Gryndler M., Schröder P., Forczek S.T., Uhlířová H., Fuksová K., Rohlenová J. (2007a): Chloroacetic acids - degradation intermediates of organic matter in forest soil. Soil Biology and Biochemistry, 39: 382-385. Go to original source...
  62. Matucha M., Gryndler M., Forczek S.T., Schröder P., Bastviken D., Rohlenová J., Uhlířová H., Fuksová K. (2007b): A chlorine-36 and carbon-14 study of the role of chlorine in the forest ecosystem. Journal of Labelled Compounds and Radiopharmaceuticals, 50: 1-3. Go to original source...
  63. Matucha M., Gryndler M., Forczek S.T., Rohlenová J., Uhlířová H., Fuksová K. (2008): Final report of the GAČR, Project No. 526/05/0636. (In Czech)
  64. Michalzik B., Tipping E., Mulder J., Gallardo Lancho J.F., Matzner E., Bryant C.L., Clarke N., Lofts S., Vicente Esteban M.A. (2003): Modelling the production and transport of disssolved organic carbon in forest soils. Biogeochemistry, 66: 241-264. Go to original source...
  65. Miller J.W., Uden P.C. (1983): Characterization of nonvolatile aqueous chlorination products of humic substance. Environmental Science and Technology, 17: 150-157. Go to original source... Go to PubMed...
  66. Myneni S.C.B. (2002): Formation of stable chlorinated hydrocar bons in weathering plant material. Science, 295: 1039-1041. Go to original source... Go to PubMed...
  67. Neal C., Rosier P.T.W. (1990): Chemical studies of chloride and stable isotopes in two conifer afforesten and moorland sites in the British uplands. Journal of Hydrology, 115: 269-283. Go to original source...
  68. Niedan V., Pavasars I., Öberg G. (2000): Chloroperoxidase-mediated chlorination of aromatic groups in fulvic acids. Chemosphere, 41: 779-785. Go to original source... Go to PubMed...
  69. Norrström A.C., Bergstedt E. (2001): The impact of road de-icing salts (NaCl) on colloid dispersion and base cation pools in roadside soils. Water, Soil, and Air Pollution, 127: 281-299. Go to original source...
  70. Öberg G. (1998): Chloride and organic chlorine in soil. Acta Hydrochimica et Hydrobiologica, 26: 137-144. Go to original source...
  71. Öberg G., Groen C. (1998a): Sources of organic halogens in spruce forest soil. Environmental Science and Technology, 32: 1573-1579. Go to original source...
  72. Öberg G., Johansen C., Groen C. (1998b): Organic halogens in spruce forest throughfall. Chemosphere, 36: 1689-1701. Go to original source...
  73. Öberg G. (2002): The natural chlorine cycle - fitting the scattered pieces. Applied Microbiology and Biotechnology, 58: 565-581. Go to original source... Go to PubMed...
  74. Öberg G. (2003): The biogeochemistry of chlorine in soil. In: Gribble G. (ed.): The Handbook of Environmental Chemistry, Vol. 3, Part P, Springer-Verlag, Berlin, 43-62. Go to original source...
  75. Öberg G., Sandén P. (2005a): Retention of chloride in soil and cycling of organic matter-bound chlorine. Hydrological Processes, 19: 2123-2136. Go to original source...
  76. Öberg G., Holm M., Sandén P., Svensson T., Parikka M. (2005b): The role of organic-matter-bound chlorine in the chlorine cycle: a case study of the Stubbertorp catchment, Sweden. Biogeochemistry, 75: 241-269. Go to original source...
  77. Ogard A.E., Thompson J.L., Rundberg R.S., Wolfsburg K., Kubik P.W., Elmore D., Bentley H.W. (1988): Migration of chlorine-36 and tritium from an underground nuclear test. Radiochimica Acta, 44/45: 213-217. Go to original source...
  78. Orcutt D.M., Nilsen E.T. (2000): Salinity Stress in Physiology of Plants under Stress. Wiley & Sons, New York, 177-235.
  79. Piccolo A. (2001): The supramolecular structure of humic substances. Soil Science, 166: 810-832. Go to original source...
  80. Piccolo A., Spaccini R., Nieder R., Richter J. (2004): Sequestration of a biologically labil organic carbon in soils by humified organic matter. Climatic Change, 67: 329-343. Go to original source...
  81. Popelkova H., Yocum C.F. (2007): Current status of the role of chloride ion in the oxygen-evolving komplex. Photosynthesis Research, 93: 111-127. Go to original source... Go to PubMed...
  82. Pracht J., Boenigk J., Isenbeck-Schröter M., Keppler F., Schöler H.F. (2001): Abiotic Fe(III) induced mineralization of phenolic substances. Chemosphere, 44: 613-619. Go to original source... Go to PubMed...
  83. Reckhow D.A., Singer P.C., Malcolm R.L. (1990): Chlorination of humic materials: by product formation and chemical interpretations. Environmental Science and Technology, 24: 1644-1655. Go to original source...
  84. Rohlenová J., Gryndler M., Forczek S.T., Fuksová K., Handová V., Matucha M. (2009): Microbial chlorination of organic matter in the forest soil: investigation using chlorine 36 and its methodology. Environmental Science and Technology, 43: 3652-3655. Go to original source... Go to PubMed...
  85. Rook J.J. (1980): Water Chlorination: Chemistry, Environmental Impact and Health Effects. In: Jolley R.L., Brungs W.A., Cumming R.B., Jacobs V.A. (eds.): Ann Argot Science, MI, Vol. 3, 85-98.
  86. Řezáčová V., Gryndler M. (2006): Fluorescence spectroscopy: a tool to characterize humic substances in soil colonized by microorganisms? Folia Microbiologica, 51: 215-221. Go to original source... Go to PubMed...
  87. Shaw P.D., Hager L.P. (1959): An enzymatic chlorination reaction. Journal of the American Chemical Society, 81: 1011-1012. Go to original source...
  88. Shaw G., Wadey P., Bell J.N.B. (2004): Radionuclide transport above a near-surface water table: IV. Soil migration and crop uptake of chlorine-36 and technetium-99, 1990 to 1993. Journal of Environmental Quality, 33: 2272-2280. Go to original source... Go to PubMed...
  89. Schlesinger W.H. (1999): Carbon sequestration in soils. Science, 284: 2095. Go to original source...
  90. Schröder P., Matucha M., Forczek S.T., Uhlířová H., Fuksová K., Albrechtová J. (2003): Uptake, translocation and fate of trichloroacetic acid in Norway spruce/soil system. Chemosphere, 52: 437-442. Go to original source... Go to PubMed...
  91. Silk P.J., Lonergan G.C., Arsenault T.L., Boyle C.D. (1997): Evidence of natural organochlorine formation in peat bogs. Chemosphere, 35: 2865-2880. Go to original source...
  92. Steinberg C.E.W., Kamara S., Prokhotskaya V.Y., Manusadžianas L., Karasyova T.A., Timofeyev M.A., Jie Z., Paul A., Meinelt T., Farjalla V.F., Matsuo A.Y.O., Burnison B.K., Menzel R. (2006): Dissolved humic substance - ecological driving forces from the individua to the ecosystems level? Freshwater Biology, 51: 1189-1210. Go to original source...
  93. Sutinen S., Juuti S., Koivisto L., Turunen M., Ruuskanen J. (1995): The uptake of and structural changes induced by trichloroacetic acid in the needles of scots pine seedlings. Journal of Experimental Botany, 46: 1223-1231. Go to original source...
  94. Svensson T., Sandén P., Bastviken D., Öberg G. (2006): Chlorine transport in a small catchment in southeast Sweden during two years. Biogeochemistry, 82: 181-199. Go to original source...
  95. Verhagen F.J.M., Swarts H.J., Wijnberg J.B.P.A., Field J.A. (1998): Organohalogen production is ubiquitous capacity among basidiomycetes. Chemosphere, 37: 2091-2104. Go to original source...
  96. Weissflog L., Krueger G., Forczek S.T., Lange Ch.A., Kotte K., Pfennigsdorff A., Rohlenová J., Fuksová K., Uhlířová H., Matucha M., Schröder P. (2007): Oxidative biodegradation of tetrachloroethene in needles of Norway spruce (Picea abies L.). South African Journal of Botany, 73: 89-96. Go to original source...
  97. Winterton N. (2000): Chlorine: the only green element-towards a wider acceptance of its role in natural cycles. Green Chemistry, 2: 173-225. Go to original source...

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