Abstract
In order to learn more about nitrogen (N) acquisition in lichens, and to see whether different lichens differ in their affinity to various N sources, N uptake was measured in 14 various lichen associations (“species”). These species represented various morphologies (fruticose or foliose), contrasting microhabitat preferences (epiphytic or terricolous), and had green algal, cyanobacterial or both forms of photobionts. N was supplied under non-limiting conditions as an amino acid mixture, ammonium, or nitrate, using 15N to quantify uptake. Carbonyl cyanide m-chlorophenylhydrazone (CCCP) was used to separate active and passive uptake. Thallus N, amino acids, soluble polyol concentrations, and the biont-specific markers chlorophyll a and ergosterol were quantified, aiming to test if these metabolites or markers were correlated with N uptake capacity. Ammonium uptake was significantly greater and to a higher extent passive, relative to the other two N sources. Nitrate uptake differed among lichen photobiont groups, cyanobacterial lichens having a lower uptake rate. All lichens had the capacity to assimilate amino acids, in many species at rates equal to nitrate uptake or even higher, suggesting that organic N compounds could potentially have an important role in the N nutrition of these organisms. There were no clear correlations between N uptake rates and any of the measured metabolites or markers. The relative uptake rates of ammonium, nitrate and amino acids were not related to morphology or microhabitat.
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Abbreviations
- CCCP:
-
Carbonyl cyanide m-chlorophenylhydrazone
- Chl:
-
Chlorophyll
- N:
-
Nitrogen
References
Ahmadjian V (1977) Qualitative requirements and utilization of nutrients: lichens. In: Rechcig M (ed) CRC handbook series in nutrition. Section D: Nutritional requirements, vol 1. Chemical Rubber Company Press, Cleveland, pp 203–215
Bhattacharya J, Singh AK, Rai AN (2002) Nitrogen nutrition in the cyanobacterium Nostoc ANTH, a symbiotic isolate from Anthoceros: Uptake and assimilation of inorganic-N and amino acids. Indian J Biochem Biol 39:163–169
Brown DH, Avalos A, Miller JE, Bargagli R (1994) Interactions of lichens with their mineral environment. Crypt Bot 4:135–142
Butler TJ, Likens GE (1995) A direct comparison of throughfall plus stemflow to estimates of dry and total deposition for sulfur and nitrogen. Atmos Environ 29:1253–1265
Carlisle A, Brown AHF, White EJ (1966) The organic matter and nutrient elements in the precipitation beneath a sessile oak (Quercus petraea) canopy. J Ecol 54; 87–98
Carlisle A, Brown AHF, White EJ (1967) The nutrient content of tree stem flow and ground flora litter and leachates in a sessile oak (Quercus petraea) woodland. J Ecol 55: 615–627
Cho B-H, Sauer N, Komor E, Tanner W (1981) Glucose induces two amino acid transport systems in Chlorella. Proc Natl Acad Sci USA 78:3591–3594
Cornell SE, Jickells TD, Cape AP, Rowland AP, Duce RA (2003) Organic nitrogen deposition on land and costal environments: a review of methods and data. Atmos Environ 37:2173–2191
Crittenden PD (1996) The effect of oxygen depravation on inorganic nitrogen uptake in an Antarctic macrolichen. Lichenologist 28:347–354
Crittenden PD (1998) Nutrient exchange in an Antarctic macrolichen during summer snowfall-snow melt events. New Phytol 139:697–707
Crittenden PD, Kalucka I, Oliver E (1994) Does nitrogen limit the growth of Lichens? Crypt Bot 4:142–155
Dahlman L, Zetherström M, Sundberg B, Näsholm T, Palmqvist K (2001) Measuring ergosterol and chitin in lichens. In: Kranner I, Beckett R, Varma A (eds) Protocols in lichenology—culturing, biochemistry, physiology and use in biomonitoring. Springer, Berlin Heidelberg New York, pp 348–362.
Dahlman L, Persson J, Näsholm T, Palmqvist K (2003) Carbon and nitrogen distribution in the green algal lichens Hypogymnia physodes and Platismatia glauca in relation to nutrient supply. Planta 217:41–48
Ekblad A, Wallander H, Näsholm T (1998) Chitin and ergosterol combined to measure total and living fungal biomass in ectomycorrhizas. New Phytol 138:143–149
Grossman A Takahasi H (2001) Macronutrient utilization by photosynthetic eukaryotes and the fabric of interactions. Annu Rev Plant Mol Biol 52:163–210
Hale ME Jr (1983) The biology of lichens, 3rd edn. Arnold, London
Honegger R (1991) Functional aspects of the lichen symbiosis. Annu Rev Plant Physiol 42:553–578
Honegger R (1993) Tansley review No 60, Developmental biology of lichens. New Phytol 125:659–677
Kielland K (1997) Role of free amino acids in the nitrogen economy of arctic cryptogams. Ecoscience 4:75–79
Kinoshita Y, Yamamoto Y, Kurokawa T, Yosihmura I (2001) Influences of nitrogen sources on usnic acid production in a cultured mycobiont of the lichen Usnea hirta (L.) Wigg. Biosci Biotechnol Biochem 65:1900–1902
Lang GE, Reiners WA, Heier RK (1976) Potential alterations of precipitation chemistry by epiphytic lichens. Oecologia 25:229–241
Lejay L, Tillard P, Lepetit M, Olive FD, Filleur S, Daniel-Vedele F, Gojon A (1999) Molecular and functional regulation of two NO3 − uptake systems by N- and C-status of Arabidopsis plants. Plant J 18:509–519
Martin J, Mahlke K, Pfanner N (1991) Role of an energized inner membrane in mitochondrial protein import. J Biochem 266:18051–18057
Marzluf GA (1981) Regulation of nitrogen metabolism and gene expression in fungi. Microbiol Rev 45:437–461
Nash TH III (ed) (1996) Lichen biology. Cambridge University Press, Cambridge, pp 303
Olsson KEA, Wallmark PH (1999) Novel calibration with correction for drift and non-linear response for continuous flow isotope ratio mass spectrometry applied to the determination of delta N-15, total nitrogen, delta C-13 and total carbon in biological material. Analyst 124:571–577
Palmqvist K (1993) Photosynthetic CO2 use in lichens and their isolated photobionts: the possible role of a CO2 concentrating mechanism in cyanobacterial lichens. Planta 191:48–56
Palmqvist K, Sundberg B (2001) Characterizing photosynthesis and respiration in freshly isolated or cultured lichen photobionts. In: Kranner I, Beckett R, Varma A (eds) Protocols in lichenology—culturing, biochemistry, physiology and use in biomonitoring. Springer, Berlin Heidelberg New York, pp 152–181
Palmqvist K, Dahlman L, Valladares F, Tehler A, Sancho LG, Mattsson J-E (2002) CO2 exchange and thallus nitrogen across 75 contrasting lichen associations from different climate zones. Oecologia. 133:295–306
Persson J, Näsholm T (2001) A GC–MS method for determination of amino acid uptake by plants. Physiol Plant 113:352–358
Persson J, Näsholm T (2002) Regulation of amino acid uptake in conifers by exogenous and endogenous nitrogen. Planta 215:639–644
Rai AN (1988) Nitrogen metabolism. In: Galun M (ed) Handbook of lichenology, vol 1. CRC Press, Boca Raton, pp 201–237
Richardson DHS (1999) War in the world of lichens: parasitism and symbiosis as exemplified by lichens and lichenicolous fungi. Mycol Res 6:641–650
Shapiro IA (1984) Activities of nitrate reductase and glutamine synthetase in lichens. Sov Plant Physiol 30:539–542
Smith DC (1960a) Studies in the physiology of lichens. 1. The effects of starvation and of ammonia absorption upon the nitrogen content of Peltigera polydactyla. Ann Bot NS 24:52–62
Smith DC (1960b) Studies in the physiology of lichens. 2, Absorption and utilization of some simple organic nitrogen compounds by Peltigera polydactyla. Ann Bot NS 24:172–185
Tehler A (1996) Systematics, phylogeny and classification. In: Nash III (ed) Lichen biology. Cambridge University Press, Cambridge, pp 217–239
Valladares F, Sancho LG (2000) The relevance of nutrient availability for lichen productivity in the Maritime Antarctic. Bibl Lichenol 75:189–199
Williams LE, Miller AJ (2001) Transporters responsible for the uptake and partitioning of nitrogenous solutes. Annu Rev Plant Physiol. Plant Mol Biol 52:659–689
Acknowledgements
The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) provided grants to K.P. (24.0795/97) and T.N. (23.0345/99). The Center for Environmental Research (CMF, Umeå, Sweden) provided a grant to L.D. (993194). Margareta Zetherström (Department of Forest Genetics and Plant Physiology, SLU, Sweden) gave skilful technical support throughout. Henrik Hedenås (Department of Ecology and Environmental Sciences, Umeå University, Sweden) is acknowledged for helping with the identification of the lichen material. Anna Crewe is acknowledged for correcting the language (Department of Ecology and Environmental Sciences, Umeå University).
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Dahlman, L., Persson, J., Palmqvist, K. et al. Organic and inorganic nitrogen uptake in lichens. Planta 219, 459–467 (2004). https://doi.org/10.1007/s00425-004-1247-0
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DOI: https://doi.org/10.1007/s00425-004-1247-0