Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-26T13:55:08.743Z Has data issue: false hasContentIssue false
  • English
  • Français

Hydrogen sulphide inhibits PSII of lichen photobionts

Published online by Cambridge University Press:  08 January 2013

Stefano BERTUZZI  and
Mauro TRETIACH
Stefano BERTUZZI
Affiliation:
Dipartimento di Scienze della Vita, Università degli Studi di Trieste, Via L. Giorgieri 10, I-34127 Trieste, Italy. Email: tretiach@units.it
Mauro TRETIACH*
Affiliation:
Dipartimento di Scienze della Vita, Università degli Studi di Trieste, Via L. Giorgieri 10, I-34127 Trieste, Italy. Email: tretiach@units.it
Get access Rights & Permissions [Opens in a new window]

Abstract

The effects of hydrogen sulphide (H2S) on five lichens with different photobionts, ecology, and tolerance to the pollutant were studied by means of samples exposed in closed chambers containing two known H2S solutions. The H2S concentration in the void volume at equilibrium with the liquid phase was measured by gas chromatography-mass spectrometry, combined with the use of solid phase micro extraction (GC/MS SPME). It was determined as 8 and 28 ppm H2S in the absence of lichen material, and c. 2 and 10 ppm H2S respectively with living lichen material inserted for 8 hours in the exposure chambers. Significant differences in the species-specific emission of chlorophyll a fluorescence (ChlaF) were observed, with a pronounced depression of Fv/Fm already detectable after 2 h exposure at 28 ppm H2S in all the species. The decreased intensity was positively correlated to sample surface and, to a lesser extent, to the species-specific pre-exposure Fv/Fm value. Dark-exposed samples were less affected than light-exposed ones. All four chlorolichens could recover the pre-exposure ChlaF emission after two days in the absence of H2S, both in the light and in the dark, whereas the cyanolichen did not recover when kept in the dark. The results are thoroughly discussed on the basis of the known action mechanisms of H2S on the photosynthetic apparatus of vascular plants and cyanobacteria.

Keywords

chlorophyll a fluorescenceFv/FmGC/MS SPMEH2Soxygen-evolving complexphotosynthesis
Type
Articles
Information
The Lichenologist , Volume 45 , Issue 1 , January 2013 , pp. 101 - 113
Copyright
Copyright © British Lichen Society 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

Arnórsson, S. (2004) Environmental impact of geothermal energy utilization. In Energy, Waste and the Environment: a Geochemical Perspective (Gieré, R. & Stille, P., eds): 297–336. London: Geological Society.Google Scholar
Arthur, C. L. & Pawliszyn, J. (1990) Solid phase microextraction with thermal desorption using fused silica optical fibers. Analytical Chemistry 62: 2145–2148.CrossRefGoogle Scholar
Axtmann, R. C. (1975) Environmental impact of a geothermal power plant. Science 187: 795–803.Google Scholar
Barber, J. (2002) Photosystem II: a multisubunit membrane protein that oxidises water. Current Opinion in Structural Biology 12: 523–530.Google Scholar
Baruffo, L. (2007) La fluorescenza clorofilliana quale nuovo strumento per la stima della vitalità lichenica nel biomonitoraggio ambientale. Ph.D. thesis, Università degli Studi di Trieste.Google Scholar
Baruffo, L. & Tretiach, M. (2007) Seasonal variations of Fo, Fm, and Fv/Fm in an epiphytic population of the lichen Punctelia subrudecta (Nyl.) Krog. Lichenologist 39: 555–565.Google Scholar
Baruffo, L., Piccotto, M. & Tretiach, M. (2008) Intrathalline variation of chlorophyll a fluorescence emission in the epiphytic lichen Flavoparmelia caperata . Bryologist 111: 455–462.CrossRefGoogle Scholar
Bates, J. W. & Brown, D. H. (1981) Epiphyte differentiation between Quercus petraea and Fraxinus excelsior trees in a maritime area of South West England. Plant Ecology 48: 61–70.Google Scholar
Beauchamp, R. O., Bus, J. S., Popp, J. A., Boreiko, C. J., Andjelkovich, D. A. & Leber, P. (1984) A critical review of the literature on hydrogen sulfide toxicity. Critical Reviews in Toxicology 13: 25–97.Google Scholar
Belkin, S. & Padan, E. (1983) Na-dithionite promotes photosynthetic sulfide utilization by the cyanobacterium Oscillatoria limnetica . Plant Physiology 72: 825–828.CrossRefGoogle ScholarPubMed
Buwalda, F., Stulen, I., Kok, L. J. & Kuiper, P. J. C. (1990) Cysteine, γ-glutamyl-cysteine and glutathione contents of spinach leaves as affected by darkness and application of excess sulfur. II. Glutathione accumulation in detached leaves exposed to H2S in the absence of light is stimulated by the supply of glycine to the petiole. Physiologia Plantarum 80: 196–204.Google Scholar
Cai, L., Koziel, J. A., Davis, J., Lo, Y. C. & Xin, H. (2006) Characterization of volatile organic compounds and odors by in-vivo sampling of beef cattle rumen gas, by solid-phase microextraction, and gas chromatography-mass spectrometry-olfactometry. Analytical and Bioanalytical Chemistry 386: 1791–1802.CrossRefGoogle ScholarPubMed
Cohen, Y., Padan, E. & Shilo, M. (1975) Facultative anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica . Journal of Bacteriology 123: 855–961.CrossRefGoogle ScholarPubMed
Cohen, Y., Jørgensen, B. B., Revsbech, N. P. & Poplawski, R. (1986) Adaptation to hydrogen sulfide of oxygenic and anoxygenic photosynthesis among cyanobacteria. Applied and Environmental Microbiology 51: 398–407.Google Scholar
Czyzewska, K. (1991) The influence of industrial air pollution forest lichens at Tomaszow Mazowiecki Region (Central Poland). Acta Mycologica 27: 247–256.Google Scholar
Degelius, G. (1964) Biological studies of the epiphytic vegetation on twigs of Fraxinus excelsior . Acta Horti Gothoburgensis 27: 25–60.Google Scholar
Degelius, G. (1978) Further studies on the epiphytic vegetation on twigs. Botanica Gothoburgensia 7: 1–58.Google Scholar
De Kok, L. J., Maas, F. M., Godeke, J., Haaksma, A. B. & Kuiper, P. J. C. (1986) Glutathione, a tripeptide which may function as a temporary storage compound of excessive reduced sulphur in H2S fumigated spinach plants. Plant and Soil 91: 349–352.Google Scholar
Deltoro, V. I., Gimeno, C., Calatayud, A. & Barreno, E. (1999) Effects of SO2 fumigations on photosynthetic CO2 gas exchange, chlorophyll a fluorescence emission and antioxidant enzymes in the lichens Evernia prunastri and Ramalina farinacea . Physiologia Plantarum 105: 648–654.Google Scholar
DeRose, V. J., Mukerji, I., Latimer, M. J, Yachandra, V. K., Sauer, K. & Klein, M. P. (1994) Comparison of the manganese oxygen-evolving complex in photosystem II of spinach and Synechococcus sp. with multinuclear manganese model compounds by X-ray absorption spectroscopy. Journal of the American Chemical Society 116: 5239–5249.CrossRefGoogle Scholar
Edwards, B., Aptroot, A., Hawksworth, D. L. & James, P. W. (2009) Lecanora Ach. in Luyken (1809). In The Lichens of Great Britain and Ireland (Smith, C. W., Aptroot, A., Coppins, B. J., Fletcher, A., Gilbert, O. L., James, P. W. & Wolseley, P. A., eds): 465–502. London: British Lichen Society.Google Scholar
Espie, G. S., Miller, A. G. & Canvin, D. T. (1989) Selective and reversible inhibition of active CO2 transport by hydrogen sulfide in a cyanobacterium. Plant Physiology 91: 387–394.Google Scholar
Fan, X. (2004) Involvement of volatile sulfur compounds in ionizing radiation-induced off-odor of fresh orange juice. Journal of Food Science 69: 593–598.Google Scholar
Genty, B., Briantais, J. M. & Baker, N. R. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990: 87–92.Google Scholar
Gries, C., Sanz, M. J. & Nash, T. H. III (1995) The effect of SO2 fumigation on CO2 gas exchange, chlorophyll fluorescence and chlorophyll degradation in different lichen species from western North America. Cryptogamic Botany 5: 239–246.Google Scholar
Hashimoto, A., Yamamoto, Y. & Theg, S. M. (1996) Unassembled subunits of the photosynthetic oxygen-evolving complex present in the thylakoid lumen are long-lived and assembly-competent. FEBS Letters 391: 29–34.Google Scholar
Koch, M. S., Mendelssohn, I. A. & McKee, K. L. (1990) Mechanism for the hydrogen sulfide-induced growth limitation in wetland macrophytes. Limnology and Oceanography 35: 399–408.Google Scholar
Kok, B., Forbush, B. & McGloin, M. (1970) Cooperation of charges in photosynthetic O2 evolution. I. A linear four step mechanism. Limnology and Oceanography 11: 457–475.Google Scholar
Laundon, J. R. (2003) Six lichens of the Lecanora varia group. Nova Hedwigia 76: 83–111.Google Scholar
Lazár, D. & Nauš, J. (1998) Statistical properties of chlorophyll fluorescence induction parameters. Photosynthetica 35: 121–127.Google Scholar
Lelieveld, J., Roelofs, G. J., Ganzeveld, L., Feichter, J. & Rodhe, H. (1997) Terrestrial sources and distribution of atmospheric sulphur. Philosophical Transactions of the Royal Society of London, Series B 352: 149–158.Google Scholar
Liu, L. N., Chen, X. L., Zhang, Y. Z. & Zhou, B. C. (2005) Characterization, structure and function of linker polypeptides in phycobilisomes of cyanobacteria and red algae: an overview. Biochimica et Biophysica Acta 1708: 133–142.Google Scholar
Loppi, S. (1996) Lichens as bioindicators of geothermal air pollution in Central Italy. Bryologist 99: 41–48.Google Scholar
Loppi, S., Cenni, E., Bussotti, F. & Ferretti, M. (1998) Biomonitoring of geothermal air pollution by epiphytic lichens and forest trees. Chemosphere 36: 1079–1082.CrossRefGoogle Scholar
Ma, H., Cheng, X., Li, G., Chen, S., Quan, Z., Zhao, S. & Niu, L. (2000) The influence of hydrogen sulfide on corrosion of iron under different conditions. Corrosion Science 42: 1669–1683.CrossRefGoogle Scholar
Maas, F. M., De Kok, L. J., Hoffmann, I. & Kuiper, P. J. C. (1987 a) Plant responses to H2S and SO2 fumigation. I. Effects on growth, transpiration and sulfur content of spinach. Plant Physiology 70: 713–721.Google Scholar
Maas, F. M., De Kok, L. J., Peters, J. L. & Kuiper, P. J. C. (1987 b) A comparative study on the effects of H2S and SO2 fumigation on the growth and accumulation of sulphate and sulphydryl compounds in Trifolium pratense L., Glycine max Merr. and Phaseolus vulgaris L. Journal of Experimental Botany 38: 1459–1469.CrossRefGoogle Scholar
Maas, F. M., van Loo, E. N. & van Hasselt, P. R. (1988) Effect of long-term H2S fumigation on photosynthesis in spinach. Correlation between CO2 fixation and chlorophyll a fluorescence. Plant Physiology 72: 77–83.Google Scholar
Miller, S. R. & Bebout, B. M. (2004) Variation in sulfide tolerance of photosystem II in phylogenetically diverse cyanobacteria from sulfidic habitats. Applied and Environmental Microbiology 70: 736–744.CrossRefGoogle ScholarPubMed
Möller, D. (1983) On the global natural sulphur emission. Atmospheric Environment 18: 29–39.Google Scholar
Nimis, P. L. & Martellos, S. (2008) ITALIC – The Information System on Italian Lichens. Version 4.0. University of Trieste, Department of Biology, IN4.0/1; http://dbiodbs.univ.trieste.it/.Google Scholar
Piccotto, M. & Tretiach, M. (2010) Photosynthesis in chlorolichens: the influence of the habitat light regime. Journal of Plant Research 123: 763–775.Google Scholar
Piccotto, M., Bidussi, M. & Tretiach, M. (2011) Effects of the urban environmental conditions on the chlorophyll a fluorescence emission in transplants of three ecologically distinct lichens. Environmental and Experimental Botany 73: 102–107.Google Scholar
Reiffenstein, R. J., Hulbert, W. C. & Roth, S. H. (1992) Toxicology of hydrogen sulfide. Annual Review of Pharmacology and Toxicology 32: 109–134.Google Scholar
Shimizu, A. (2004) Community structure of lichens in the volcanic highlands of Mt. Tokachi, Hokkaido, Japan. Bryologist 107: 141–151.Google Scholar
Sivaraja, M., Hunziker, D. & Dismukes, G. C. (1988) The reaction of H2S with the photosynthetic water-oxidizing complex and its lack of reaction with the primary electron acceptor in spinach. Biochimica et Biophysica Acta 936: 228–235.Google Scholar
Stuiver, C. E. E. & De Kok, L. J. (2001) Atmospheric H2S as sulfur source for Brassica oleracea: kinetics of H2S uptake and activity of O-acetylserine (thiol)lyase as affected by sulfur nutrition. Environmental and Experimental Botany 46: 29–36.Google Scholar
Sundberg, B., Campbell, D. & Palmqvist, K. (1997) Predicting CO2 gain and photosynthetic light acclimation from fluorescence yield and quenching in cyano-lichens. Planta 201: 138–145.CrossRefGoogle Scholar
Tandeau de Marsac, N. & Cohen-Bazire, G. (1977) Molecular composition of cyanobacterial phycobilisomes. Proceedings of the National Academy of Sciences of the United States of America 74: 1635–1639.Google Scholar
Thompson, C. R. & Kats, G. (1978) Effects of continuous hydrogen sulfide fumigation on crop and forest plants. Environmental Science and Technology 12: 550–553.CrossRefGoogle Scholar
Tretiach, M. & Baruffo, L. (2001) Effects of H2S on CO2 gas exchanges and growth rates of the epiphytic lichen Parmelia sulcata Taylor. Symbiosis 31: 35–46.Google Scholar
Tretiach, M. & Ganis, P. (1999) Hydrogen sulphide and epiphytic lichen vegetation: a case study on Mt. Amiata (Central Italy). Lichenologist 31: 163–181.Google Scholar
Tretiach, M., Monaci, F., Baruffo, L. & Bargagli, R. (1999) Effetti dell'H2S sul contenuto di elementi in tracce nel lichene epifita Parmelia sulcata . Bollettino della Società Adriatica di Scienze 78: 365–387.Google Scholar
Tretiach, M., Crisafulli, P., Pittao, E., Rinino, S., Roccotiello, E. & Modenesi, P. (2005) Isidia ontogeny and its effect on the CO2 gas exchanges of the epiphytic lichen Pseudevernia furfuracea (L.) Zopf. Lichenologist 37: 445–462.Google Scholar
Tretiach, M., Adamo, P., Bargagli, R., Baruffo, L., Crisafulli, P., Giordano, S., Modenesi, P., Orlando, S. & Pittao, E. (2007 a) Lichen and moss bags as monitoring devices in urban areas, part I: influence of exposure on vitality. Environmental Pollution 146: 380–391.Google Scholar
Tretiach, M., Piccotto, M. & Baruffo, L. (2007 b) Effects of ambient NO X on chlorophyll a fluorescence in transplanted Flavoparmelia caperata (Lichen). Environmental Science and Technology 41: 2978–2984.Google Scholar
Vazquez-Landaverde, P. A., Qian, M. C. & Torres, J. A. (2007) Kinetic analysis of volatile formation in milk subjected to pressure-assisted thermal treatments. Journal of Food Science 72: 389–498.Google Scholar
Vitikainen, O. (1994) Taxonomic revision of Peltigera (lichenized Ascomycota) in Europe. Acta Botanica Fennica 152: 1–96.Google Scholar
Warneck, P. (2000) Sulfur compounds in the atmosphere. In Chemistry of the Natural Atmosphere. International Geophysics Series 71 (Warneck, P., ed): 587–655. San Diego: Academic Press.Google Scholar
Westerman, S., Stulen, I., Suter, M., Brunold, C. & De Kok, L. J. (2001) Atmospheric H2S as sulphur source for Brassica oleracea: consequences for the activity of the enzymes of the assimilatory sulphate reduction pathway. Plant Physiology and Biochemistry 39: 425–432.Google Scholar