biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 53:214-222, 2009 | DOI: 10.1007/s10535-009-0042-y

Interactions of lichens with heavy metals

M. Bačkor1,*, S. Loppi2
1 Institute of Biology and Ecology, Department of Botany, Šafárik University, Košice, Slovak Republic
2 Department of Environmental Science, G. Sarfatti University of Siena, Siena, Italy

Recent developments in knowledge about the interactions between lichens and heavy metals at different levels, from populations to cells and from ecology to molecular biology are reviewed. Sources of heavy metals, mechanisms of heavy metal accumulation and detoxification by lichens are discussed. Special emphasis is placed on ultrastructural changes as well as physiological parameters such as membrane integrity, pigment composition, chlorophyll a fluorescence, photosynthesis, respiration, contents of ATP, amino acids, ergosterol, ethylene, non-protein thiols, activity of antioxidant enzymes and expression of stress proteins.

Keywords: biomonitoring; cadmium; copper; detoxification; exclusion; lead; manganese; mercury; zinc
Subjects: heavy metals; lichen

Received: June 10, 2008; Accepted: December 2, 2008; Published: June 1, 2009  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Bačkor, M., & Loppi, S. (2009). Interactions of lichens with heavy metals. Biologia plantarum, 53(2), 214-222. doi: 10.1007/s10535-009-0042-y
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Adamo, P., Crisafulli, P., Giordano, S., Minganti, V., Modenesi, P., Monaci, F., Pittao, E., Tretiach, M., Bargagli, R.: Lichen and moss bags as monitoring devices in urban areas. Part II: Trace element content in living and dead biomonitors and comparison with synthetic materials.-Environ. Pollut. 146: 392-399, 2007. Go to original source...
    2. Bačkor, M., Dzubaj, A.: Short-term and chronic effects of copper, zinc and mercury on the chlorofyll content of four lichen photobionts and related alga.-J. Hattori bot. Lab. 95: 271-283, 2004.
    3. Bačkor, M., Fahselt, D.: Using EDX-micronalysis and X-ray mapping to demonstrate metal uptake by lichens.-Biologia 59: 39-45, 2004a.
    4. Bačkor, M., Fahselt, D.: Physiological attributes of the lichen Cladonia pleurota in metal-rich and control sites near Sudbury (Ontario, Canada).-Environ. exp. Bot. 52: 149-159, 2004b. Go to original source...
    5. Bačkor, M., Fahselt, D.: Tetrazolium reduction as an indicator of environmental stress in lichens and isolated bionts.-Environ. exp. Bot. 53: 125-133, 2005. Go to original source...
    6. Bačkor, M., Fahselt, D., Davidson, R.D., Wu, C.T.: Effects of copper on wild and tolerant strains of the lichen photobiont Trebouxia erici (Chlorophyta) and possible tolerance mechanisms.-Arch. environ. Contam. Toxicol. 45: 159-167, 2003. Go to original source...
    7. Bačkor, M., Fahselt, D., Wu, C.T.: Free proline content is positively correlated with copper tolerance of the lichen photobiont Trebouxia erici (Chlorophyta).-Plant Sci. 167: 151-157, 2004. Go to original source...
    8. Bačkor, M., Gibalová, A., Bud'ová, J., Mikeš, J., Solár, P.: Cadmium-induced stimulation of stress-protein hsp70 in lichen photobiont Trebouxia erici.-Plant Growth Regul. 50: 159-164, 2006b. Go to original source...
    9. Bačkor, M., Hudák, J., Repčák, M., Ziegler, W., Bačkorová, M.: The influence of pH and lichen metabolites (vulpinic acid and (+) usnic acid) on the growth of lichen photobiont Trebouxia irregularis.-Lichenologist 30: 577-582, 1998. Go to original source...
    10. Bačkor, M., Pawlik-Skowrońska, B., Bud'ová, J., Skowroński, T.: Response to copper and cadmium stress in wild-type and copper tolerant strains of the lichen alga Trebouxia erici: metal accumulation, toxicity and non-protein thiols.-Plant Growth Regul. 52: 17-27, 2007b. Go to original source...
    11. Bačkor, M., Pawlik-Skowrońska, B., Tomko, J., Bud'ová, J., Sanità di Toppi, L.: Response to copper stress in aposymbiotically grown lichen mycobiont Cladonia cristatella: uptake, viability, ergosterol and production of non-protein thiols.-Mycol. Res. 110: 994-999, 2006a. Go to original source...
    12. Bačkor, M., Váczi, P., Barták, M., Bud'ová, J., Dzubaj, A.: Uptake, photosynthetic characteristics and membrane lipid peroxidation levels in the lichen photobiont Trebouxia erici exposed to copper and cadmium.-Bryologist 110: 100-107, 2007a. Go to original source...
    13. Bačkor, M., Zetíková, J.: Effects of copper, cobalt and mercury on the chlorophyll content of lichens Cetraria islandica and Flavocetraria cucullata.-J. Hattori bot. Lab. 93: 175-187, 2003.
    14. Banásová, V., Horák, O., Čiamporová, M., Nadubinská, M., Lichtscheidl, I.: The vegetation of metalliferous and non-metalliferous grasslands in two former mine regions in Central Slovakia.-Biologia 61: 433-439, 2006. Go to original source...
    15. Bargagli, R., Iosco, F.P., Damato, M.L.: Zonation of trace metal accumulation in 3 species of epiphytic lichens belonging to the genus Parmelia.-Cryptogamie Bryol. Lichnol. 8: 331-337, 1987.
    16. Bargagli, R., Mikhailova, I.: Accumulation of inorganic contaminants.-In: Nimis, P.L., Scheidegger, C., Wolseley, P.A. (ed.): Monitoring with Lichens-Monitoring Lichens. Pp. 65-84. Kluwer Academic Publishers, Dordrecht-Boston-London 2002. Go to original source...
    17. Barnes, J.D., Balaguer, L., Manrique, E., Elvira, S., Davison, A.V.: A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants.-Environ. exp. Bot. 32: 85-100, 1992. Go to original source...
    18. Bergamaschi, L., Rizzio, E., Giaveri, G., Loppi, S., Gallorini, M.: Comparison between the accumulation capacity of four lichen species transplanted to a urban site.-Environ. Pollut. 148: 468-476, 2007. Go to original source...
    19. Bierkens, J.G.E.A.: Applications and pitfalls of stress proteins in biomonitoring.-Toxicology 153: 61-72, 2000. Go to original source...
    20. Boonpragob, K.: Monitoring physiological change in lichens: total chlorophyll content and chlorophyll degradation.-In: Nimis, P.L., Scheidegger, C., Wolseley, P.A. (ed.): Monitoring with Lichens-Monitoring Lichens. Pp. 323-326. Kluwer Academic Publishers, Dordrecht-Boston-London 2002. Go to original source...
    21. Boonpragob, K., Nash, T.H.: Seasonal variation of elemental status in the lichen Ramalina menziesii Tayl. from 2 sites in southern California - evidence for dry deposition accumulation.-Environ. exp. Bot. 30: 415-428, 1990. Go to original source...
    22. Bradford, M.M.: A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.-Anal. Biochem. 72: 248-254, 1976. Go to original source...
    23. Branquinho, C., Brown, D.H., Catarino, F.: The cellular location of Cu in lichens and its effects on membrane integrity and chlorophyll fluorescence.-Environ. exp. Bot. 38: 165-179, 1997. Go to original source...
    24. Branquinho, C., Catarino, F., Brown, D.H., Pereira, M.J., Soares, A.: Improving the use of lichens as biomonitors of atmospheric metal pollution.-Sci. total Environ. 232: 67-77, 1999. Go to original source...
    25. Brown, D.H., Beckett, R.P.: Minerals and lichens: localisation and effect.-In: Vicente, C., Brown, D.H., Legaz, M.E. (ed.): Surface Physiology of Lichens. Pp. 127-149. Universidad Complutense de Madrid, Madrid 1985.
    26. Brown, D.H., Brown, R.M.: Mineral cycling and lichens - the physiological basis.-Lichenologist 23: 293-307, 1991. Go to original source...
    27. Bud'ová, J., Bačkor, M., Bačkorová, M., Židzik, J.: Usnic acid and copper toxicity in aposymbiotically grown lichen photobiont Trebouxia erici.-Symbiosis 42: 169-174, 2006.
    28. Carreras, H.A., Wannaz, E.D., Perez, C.A., Pignata, M.L.: The role of urban air pollutants on the performance of heavy metal accumulation in Usnea amblyoclada.-Environ. Res. 97: 50-57, 2005. Go to original source...
    29. Chettri, M.K., Cook, C.M., Vardaka, E., Sawidis, T., Lanaras, T.: The effect of Cu, Zn and Pb on the chlorophyll content of the lichen Cladonia convoluta and Cladonia rangiformis.-Environ. exp. Bot. 39: 1-10, 1998. Go to original source...
    30. Chisholm, J.E., Jones, G.C., Purvis, O.W.: Hydrated copper oxalate, moolooite, in lichens.-Mineral. Mag. 51: 715-718, 1987. Go to original source...
    31. Collins, C.R., Farrar, J.F.: Structural resistance to mass transfer in the lichen Xanthoria parietina.-New Phytol. 81: 71-83, 1978. Go to original source...
    32. Cuny, D., Davranche, L., Thomas, P., Kempa, M., Van Haluwyn, C.: Spatial and temporal variations of trace element contents in Xanthoria parietina thalli collected in a highly industrialized area in northern France as an element for a future epidemiological study.-J. Atmos. Chem. 49: 391-401, 2004. Go to original source...
    33. Dzubaj, A., Bačkor, M., Tomko, J., Peli, E., Tuba, Z.: Tolerance of the lichen Xanthoria parietina (L.) Th. Fr. to metal stress.-Ecotoxicol. environ. Safe 70: 319-326, 2008. Go to original source...
    34. Fahselt, D.: Secondary biochemistry of lichens.-Symbiosis 16: 117-165, 1994.
    35. Garty, J.: Biomonitoring atmospheric heavy metals with lichens: theory and application.-Crit. Rev. Plant Sci. 20: 309-371, 2001. Go to original source...
    36. Garty, J., Galun, M., Kessel, M.: Localization of heavy metals and other elements accumulated in the lichen thallus.-New Phytol. 82: 159-168, 1979. Go to original source...
    37. Garty, J., Karary, Y., Harel, J., Lurie, S.: Temporal and spatial fluctuations of ethylene production and concentrations of sulfur, sodium, chlorine and iron on/in the thallus cortex in thelichen Ramalina duriaei (De Not.) Bagl.-Environ. exp. Bot. 33: 553-563, 1993. Go to original source...
    38. Garty, J., Kardish, N., Hagemeyer, J., Ronen, R.: Correlations between the concentration of adenosine triphosphate, chlorophyll degradation and the amounts of airborne heavy metals and sulphur in a transplanted lichen.-Arch. environ. Contam. Toxicol. 17: 601-611, 1988. Go to original source...
    39. Garty, J., Tamir, O., Levin, T., Lehr, H.: The impact of UV-B and sulphur-or copper-containing solutions in acidic conditions on chloropfyll fluorescence in selected Ramalina species.-Environ. Pollut. 145: 266-273, 2007. Go to original source...
    40. González, C.M., Pignata, M.L.: Chemical response of the lichen Punctelia subrudecta (Nyl.) Krog transplanted close to a power station in an urban-industrial environment.-Environ. Pollut. 97: 195-203, 1997. Go to original source...
    41. Goyal, R., Seaward, M.R.D.: Metal uptake in terricolous lichens. III. Translocation in the thallus of Peltigera canina.-New Phytol. 90: 85-98, 1982a. Go to original source...
    42. Goyal, R., Seaward, M.R.D.: Metal uptake in terricolous lichens. II. Effects on the morphology of Peltigera canina and Peltigera rufescens.-New Phytol. 90: 73-84, 1982b. Go to original source...
    43. Grill, E., Winnacker, E.L., Zenk, M.H.: Phytochelatins: the principal heavy-metal complexing peptides of higher plants.-Science 230: 674-676, 1985. Go to original source...
    44. Gushina, I.A., Harwood, J.L.: Lead and copper effects on lipid metabolism in cultured lichen photobionts with different phosphorus status.-Phytochemistry 67: 1731-1739, 2006. Go to original source...
    45. Hare, P.D., Cress, W.A.: Metabolic implications of stress-induced proline accumulation in plants.-Plant Growth Regul. 21: 79-102, 1997. Go to original source...
    46. Hauck, M., Huneck, S.: Lichen substances affect metal adsorption in Hypogymnia physodes.-J. chem. Ecol. 33: 219-223, 2007. Go to original source...
    47. Hauck, M., Paul, A.: Manganese as a site factor for epiphytic lichens.-Lichenologist 37: 409-423, 2005. Go to original source...
    48. Knops, J.M.H., Nash, T.H., Boucher, V.L., Schlesinger, W.H.: Mineral cycling and epiphytic lichens-implications at the ecosystem level.-Lichenologist 23: 309-321, 1991. Go to original source...
    49. Král, R., Kryžová, L., Liška, J.: Background concentrations of lead and cadmium in the lichen Hypogymnia physodes at different altitudes.-Sci. total Environ. 84: 201-209, 1989. Go to original source...
    50. Larson, D.W.: The absorption and release of water by lichens.-In: Peveling, E. (ed.): Progress and Problems in Lichenology in the Eighties. Pp. 351-260. J. Cramer, Berlin-Stuttgart 1987.
    51. Loppi, S., Nelli, L., Ancora, S., Bargagli, R.: Accumulation of trace elements in the peripheral and central parts of a foliose lichen thallus.-Bryologist 100: 251-253, 1997. Go to original source...
    52. Loppi, S., Pirintsos, S.A., De Dominicis, V.: Soil contribution to the elemental composition of epiphytic lichens (Tuscany, central Italy).-Environ. Monit. Assess. 58: 121-131, 1999. Go to original source...
    53. Marques, A.P., Freitas, M.C., Wolterbeek, H.T., Steinebach, O.M., Verburg, T., De Goeij, J.J.M.: Cell-membrane damage and element leaching in transplanted Parmelia sulcata lichen related to ambient SO2, temperature, and precipitation.-Environ. Sci. Technol. 39: 2624-2630, 2005. Go to original source...
    54. May, M.J., Vernoux, T., Leaver, C., Van Montagu, M., Inze, D.: Glutathione homeostasis in plants: implications for environmental sensing and plant development.-J. exp. Bot. 49: 649-667, 1998. Go to original source...
    55. Mikhailova, I.N.: Populations of epiphytic lichens under stress conditions: survival strategies.-Lichenologist 39: 83-89, 2007. Go to original source...
    56. Mittra, B., Sharma, S., Das, A.B., Henry, S.L., Das, T.K., Ghosh, P., Ghosh, S, Mohanty, P.: A novel cadmium induced protein in wheat: characterization and localization in root tissue.-Biol. Plant. 52: 343-346, 2008. Go to original source...
    57. Monnet, F., Bordas, F., Deluchat, V., Baudu, M.: Toxicity of copper excess on the lichen Dermatocarpon luridum: antioxidant enzyme activities.-Chemosphere 65: 1806-1813, 2006. Go to original source...
    58. Monnet, F., Bordas, F, Deluchat, V., Chatenet, P., Botineau, M., Baudu, M.: Use of the aquatic lichen Dermatocarpon luridum as bioindicator of copper pollution: accumulation and cellular distribution tests.-Environ. Pollut. 138: 455-461, 2005. Go to original source...
    59. Nash, T.H.: Metal tolerance in lichens.-In: Shaw, A.J. (ed): Heavy Metal Tolerance in Plants: Evolutionary Aspects. Pp. 119-131. CRC Press, Boca Raton 1989.
    60. Nash, T.H.: Nutrients, elemental accumulation and mineral cycling.-In: Nash, T.H. (ed.): Lichen Biology. Pp. 136-153. University Press, Cambridge 1996.
    61. Nash, T.H., Gries, C.: The use of lichens in atmospheric deposition studies with an emphasis on the Arctic.-Sci. total. Environ. 160/161: 729-736, 1995. Go to original source...
    62. Nieboer, E., Puckett, K.J., Grace, B.: The uptake of nickel by Umbilicaria muhlenbergii a physicochemical process.-Can. J. Bot. 54: 724-733, 1976. Go to original source...
    63. Nieboer, E., Richardson, D.H.S., Tomassini, F.D.: Mineral uptake and release by lichens an overview.-Bryologist 81: 226-246, 1978. Go to original source...
    64. Panda, S.K.: Impact of copper on reactive oxygen species, lipid peroxidation and antioxidants in Lemna minor.-Biol. Plant. 52: 561-564, 2008. Go to original source...
    65. Paul, A., Hauck, M., Langenfeld-Heyser, R.: Ultrastructural changes in soredia of the epiphytic lichen Hypogymnia physodes cultivated with manganese.-Environ. exp. Bot. 52: 139-147, 2004. Go to original source...
    66. Pawlik-Skowrońska B., Purvis O.W., Pirszel J., Skowroński T.: Cellular mechanisms of Cu-tolerance in the epilithic lichen Lecanora polytropa growing at a copper mine.-Lichenologist 38: 267-275, 2006. Go to original source...
    67. Pawlik-Skowrońska, B., Sanità di Toppi, L., Favali, M.A., Fossati, F., Pirszel, J., Skowroński, T.: Lichens respond to heavy metals by phytochelatin synthesis.-New Phytol. 156: 95-102, 2002. Go to original source...
    68. Perales-Vela, H.V., Peña-Castro, J.M., Cañizares-Villanueva, R.O.: Heavy metal detoxification in eukaryotic microalgae.-Chemosphere 64: 1-10, 2006. Go to original source...
    69. Pirintsos, S.A., Matsi, T., Vokou, D., Gaggi, C., Loppi, S.: Vertical distribution patterns of trace elements in an urban environment as reflected by their accumulation in lichen transplants.-J. Atmos. Chem. 54: 121-131, 2006. Go to original source...
    70. Puckett, K.J.: The effect of heavy metals on some aspects of lichen physiology.-Can. J. Bot. 54: 2695-2703, 1976. Go to original source...
    71. Purvis, O.W.: The occurrence of copper oxalate in lichens growing on copper sulphide-bearing rocks in Scandinavia.-Lichenologist 16: 197-204, 1984. Go to original source...
    72. Purvis, O.W., Elix, J.A., Broomhead, J.A., Jones, G.C.: The occurrence of copper-norstictic acid in lichens from cupriferous substrata.-Lichenologist 19: 193-203, 1987. Go to original source...
    73. Purvis, O.W., Halls, C.: A review of lichens in metal-enriched environments.-Lichenologist 28: 571-601, 1996. Go to original source...
    74. Reis, M.A., Alves, L.C., Freitas, M.C., Van Os, B., Wolterbeek, H.T.: Lichens (Parmelia sulcata) time response model to environmental elemental availability.-Sci. total Environ. 232: 105-115, 1999. Go to original source...
    75. Richardson, D.H.S.: Metal uptake in lichens.-Symbiosis 18: 119-127, 1995.
    76. Rodriguez, J.H., Carreras, H.A., Pignata, M.L., Gonzalez, C.M.: Nickel exposure enhances the susceptibility of lichens Usnea amblyoclada and Ramalina celastri to urban atmospheric pollutants.-Arch. environ. Contam. Toxicol. 53: 533-540, 2007. Go to original source...
    77. Ronen, R., Galun, M.: Pigment extraction from lichens with dimethyl sulfoxide (DMSO) and estimation of chlorophyll degradation.-Environ. exp. Bot. 24: 239-245, 1984. Go to original source...
    78. Sanità di Toppi, L., Gremigni, P., Pawlik-Skowrońska, B., Prasad, M.N.V., Cobbett, C.S.: Response to heavy metals in plants: a molecular approach.-In: Sanità di Toppi, L., Pawlik-Skowrońska, B. (ed.): Abiotic Stresses in Plants. Pp. 133-156. Kluwer Academic Publishers, Dordrecht-Boston-London 2003. Go to original source...
    79. Sanità di Toppi, L., Marabottini, R., Vattuone, Z., Musetti, R., Favali, M.A., Sorgonà, A., Badiani, M.: Cell wall immobilization and antioxidant status of Xanthoria parietina thalli exposed to cadmium.-Funct. Plant Biol. 32: 611-618, 2005a. Go to original source...
    80. Sanità di Toppi, L., Musetti, R., Marabottini, R., Corradi, M.G., Vattuone, Z., Favali, M.A., Badiani, M.: Responses of Xanthoria parietina thalli to environmentally relevant concentrations of hexavalent chromium.-Funct. Plant Biol. 31: 329-338, 2004. Go to original source...
    81. Sanità di Toppi, L., Musetti, R., Vattuone, Z., Pawlik-Skowrońska, B., Fossati, F., Bertoli, L., Badiani, M., Favali, M.A.: Cadmium distribution and effects on ultrastructure and chlorophyll status in photobionts and mycobionts of Xanthoria parietina.-Microscop. Res. Techn. 66: 229-238, 2005b. Go to original source...
    82. Sarret, G., Manceau, A., Cuny, D., Van Haluwyn, C., Déruelle, S., Hazemann, J.L., Soldo, Y., Eybert-Bérard, L., Menthonnex, J.J.: Mechanisms of lichen resistance to metallic pollution.-Environ. Sci. Technol. 32: 3325-3330, 1998. Go to original source...
    83. Shah, K., Nongkynrih, J.M.: Metal hyperaccumulation and bioremediation.-Biol. Plant. 51: 618-634, 2007. Go to original source...
    84. Shamsi, I.H., Wei, K., Zhang, G.P., Jilani, G.H., Hassan, M.J.: Interactive effects of cadmium and aluminum on growth and antioxidative enzymes in soybean.-Biol. Plant. 52: 165-169, 2008. Go to original source...
    85. Silberstein, L., Siegel, B.Z., Siegel, S.M., Mukhtar, A., Galun, M.: Comparative studies on Xanthoria parietina, a pollution-resistant lichen, and Ramalina duriaei, a sensitive species. 1. Effects of air pollution on physiological processes.-Lichenologist 28: 355-365, 1996. Go to original source...
    86. Sundberg, B., Ekblad, A., Nasholm, T., Palmqvist, K.: Lichen respiration in relation to active time, temperature, nitrogen and ergosterol concentrations.-Funct. Ecol. 13: 119-125, 1999. Go to original source...
    87. Tarhanen, S.: Ultrastructural responses of the lichen Bryoria fuscescens to simulated acid rain and heavy metal deposition.-Ann. Bot. 82: 735-746, 1998. Go to original source...
    88. Tarhanen, S., Metsarinne, S., Holopainen, T., Oksanen, J.: Membrane permeability response of lichen Bryoria fuscescens to wet deposited heavy metals and acid rain.-Environ. Pollut. 104: 121-129, 1999. Go to original source...
    89. Towill, L.E., Mazur, P.: Studies on the reduction of 2,3,5-triphenyltetrazolium chloride as a viability assay for plant tissue cultures.-Can. J. Bot. 53: 1097-1102, 1975. Go to original source...
    90. Tretiach, M., Baruffo, L.: Effects of H2S on CO2 gas exchanges and growth rates of the epiphytic lichen Parmelia sulcata Taylor.-Symbiosis 31: 35-46, 2001.
    91. Walther, D.A., Ramelov, G.J., Beck, J.N., Young, J.C., Callahan, J.D., Marcon, M.F.: Temporal changes in metal levels of the lichen Parmotrema praesorediosum and Ramalina stenospora, southwest Louisiana.-Water Air Soil Pollut. 53: 189-200, 1990. Go to original source...
    92. Yang, X., Feng, Y., He, Z., Stoffella, P.J.: Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation.-J. trace Elements Med. Biol. 18: 339-353, 2005. Go to original source...

    Return to the content