Nitrogen and carbon isotope variability in the green-algal lichen Xanthoria parietina and their implications on mycobiont-photobiont interactions

Ecology and Evolution

Volumn 2, Issue 12, 2012, Pages 3132-3144

  Beck, Andreas ^a,b   Mayr, Christoph ^b,c  

^a BAVARIAN NATURAL HISTORY COLLECTIONS   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Lichen symbiosis; Mycobiont; Photobiont; Stable isotope; Substrate; Xanthoria parietina

Indexed keywords

EID: 84890745483     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.417     Document Type: Article

References (72)

1. Ahmadjian, V. 1965. Lichens. Annu. Rev. Microbiol. 19:1-20.
2. Batts, J. E., L. J. Calder, and B. D. Batts. 2004. Utilizing stable isotope abundances of lichens to monitor environmental change. Chem. Geol. 204:345-368.
3. Beck, A., and H. U. Koop. 2001. Analysis of the photobiont population in lichens using a single-cell manipulator. Symbiosis 31:57-67.
4. Broadmeadow, M. S. J., H. Griffiths, C. Maxwell, and A. M. Borland. 1992. The carbon isotope ratio of plant organic material reflects temporal and spatial variations in CO2 within tropical forest formations in Trinidad. Oecologia 89:435-441.
5. Cornell, S., A. Rendell, and T. Jickells. 1995. Atmospheric inputs of dissolved organic nitrogen to the oceans. Nature 376:243-246.
6. Crittenden, P. D. 1989. Nitrogen relations of mat-forming lichens. Pp. 243-268 in L. Body, R. Marchant, and D. J. Read, eds. Nitrogen, phosphorous and sulphur utilization by fungi. Cambridge Univ. Press, NY.
7. Crittenden, P. D. 1998. Nutrient exchange in an Antarctic macrolichen during summer snowfall-snow melt events. New Phytol. 139:697-707.
8. Crittenden, P. D., I. Kalucka, and E. Oliver. 1994. Does nitrogen limit the growth of lichens? Cryptogam. Bot. 4:142-155.
9. 13C of lichens. Isot. Environ. Health Stud. 43:95-104.
10. Dahlman, L., J. Persson, T. Näsholm, and K. Palmquist. 2003. Carbon and nitrogen distribution in the green algal lichens Hypogymnia physodes and Platismatia glauca in relation to nutrient supply. Planta 217:41-48.
11. Dahlman, L., J. Persson, K. Palmquist, and T. Näsholm. 2004. Organic and inorganic nitrogen uptake in lichens. Planta 219:459-467.
12. Dawson, T. E., S. Mambelli, A. H. Plamboeck, P. H. Templer, and K. P. Tu. 2002. Stable isotopes in plant ecology. Annu. Rev. Ecol. Syst. 33:507-559.
13. Dolnik, C., A. Beck, and D. Zarabska. 2010. Distinction of Cladonia reiandCladonia subulata basedonmolecular, chemical and morphological characters. Lichenologist 42:373-386.
14. Eisenreich, W., N. Knispel, and A. Beck. 2011. Advanced methods for the study of the chemistry and the metabolism of lichens. Phytochem. Rev. 10:445-456.
15. 15N in mat-forming lichens. Oecologia 136:115-123.
16. 15N natural abundance. Oecologia 117:187-193.
17. Evans, R. D. 2001. Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci. 6:121-126.
18. Farquhar, G. D., J. R. Ehleringer, and K. T. Hubick. 1989. Carbon isotope discrimination and photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40:503-537.
19. Felsenstein, J. 1985. Confidence-limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791.
20. Fogel, M. L., and L. A. Cifuentes. 1993. Isotopic fractionation during primary production. Pp. 73-98 in M. Engel and S. A. Macko, eds. Organic geochemistry. Plenum Press, New York.
21. 15N) of mangroves and lichens in an oligotrophic, microbially-influenced ecosystem. Biogeosci. Discuss. 5:937-969.
22. Fontaniella, B., M. C. Molina, and C. Vicente. 2000. An improved method for the separation of lichen symbionts. Phyton 40:323-328.
23. Forman, R. T. T. 1975. Canopy lichens with blue-green algae: A nitrogen source in a Colombian rain forest. Ecology 56:1176-1184.
24. 14N ratios in atmospheric nitrate species. Tellus 43B:30-44.
25. Galimov, E. M. 2000. Carbon isotope composition of Antarctic plants. Geochim. Cosmochim. Acta 64:1737-1739.
26. Garvie, L. A. J., L. P. Knauth, F. Bungartz, S. Klonowski, and T. H. Nash. 2008. Life in extreme environments: survival strategy of the endolithic desert lichen Verrucaria rubrocincta. Naturwissenschaften 95:705-712.
27. Guindon, S., and O. Gascuel. 2003. A simple, fast and accurate method to estimate large phylogenies by maximumlikelihood. Syst. Biol. 52:696-704.
28. Heaton, T. H. E. 1986. Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere - a review. Chem. Geol. 59:87-102.
29. Heaton, T. H. E., B. Spiro, S. Madeline, and C. Robertson. 1997. Potential canopy influences on the isotopic composition of nitrogen and sulphur in atmospheric deposition. Oecologia 109:600-607.
30. Hietz, P., W. Wanek, R. Wania, and N. M. Nadkarni. 2002. Nitrogen-15 natural abundance in a montane cloud forest canopy as an indicator of nitrogen cycling and epiphyte nutrition. Oecologia 131:350-355.
31. 15N in nitrogen-limited forests and tundra can estimate nitrogen cycling through mycorrhizal fungi: a review. Ecosystems 11:815-830.
32. Hoering, T. C., and H. T. Ford. 1960. The isotope effect in the fixation of nitrogen by Azotobacter. J. Am. Chem. Soc. 82:376-378.
33. Högberg, H. 1997. Tansley Review No. 95 - N-15 natural abundance in soil-plant systems. New Phytol. 137:179-203.
34. Honegger, R. 1991. Functional aspects of the lichen symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42:553-578.
35. Hübner, H. 1986. Isotope effects of nitrogen in the soil and biosphere. Pp. 361-425 in P. Fritz and J. C. Fontes, eds. Handbook of environmental isotope geochemistry Vol. 2. Elsevier, Amsterdam, the Netherlands.
36. Krouse, H. R. 1977. Sulphur isotope abundances elucidate uptake of atmospheric sulphur emissions by vegetation. Nature 265:45-46.
37. 13C systematics of the lichens Ramalina celastri and Ramalina subfraxinea var. confirmata, coastal Eastern Australia and adjacent hinterland. Pp. 69-70 in B. G. K. van Aarsen, ed. Australian organic geochemistry conference abstracts. Fremantle, Washington.
38. 3) on terrestrial vegetation: A review. Environ. Pollut. 124: 179-221.
39. 18O of lichens can be used as tracers of micro-environmental carbon and water sources. Pp. 77-92 in T. Dawson and R. Siegwolf, eds. Isotopes as tracer of ecological change. Chapter 6. Academic Press, Amsterdam, the Netherlands.
40. Lange, O. L., T. G. A. Green, and H. Ziegler. 1988. Water status related photosynthesis and carbon isotope discrimination in species of the lichen genus Pseudocyphellaria with green or blue-green photobionts and in photosymbiodemes. Oecologia 75:494-501.
41. Lange, O. L., T. G. A. Green, and U. Heber. 2001. Hydrationdependent photosynthetic production of lichens: What do laboratory studies tell us about field performance? J. Exp. Bot. 52:2033-2042.
42. Lindblom, L., and S. Ekman. 2005. Molecular evidence supports the distinction between Xanthoria parietina and X. aureola (Teloschistaceae, lichenized Ascomycota). Mycol. Res. 109:187-199.
43. Lindblom, L., and S. Ekman. 2007. New evidence corroborates population differentiation in Xanthoria parietina. Lichenologist 39:259-271.
44. Máguas, C., H. Griffiths, J. Ehleringer, and J. Serôdio. 1993. Characterization of photobiont associations in lichens using carbon isotope discrimination techniques. Pp. 201-212 in J. Ehleringer, A. Hall, and J. Farquhar, eds. Stable isotopes and plant carbon-water relations. Academic Press, New York.
45. 2-concentrating mechanisms and diffusion limitation. Planta 196:95-102.
46. Marshall, J. D., J. R. Brooks, and K. Lajtha. 2007. Sources of variation in the stable isotopic composition of plants. Pp. 22-60 in R. Michener and K. Lajtha, eds. Stable isotopes in ecology and environmental science. 2nd ed. Blackwell Publishing, Malden, MA.
47. Matzek, V., and P. Vitousek. 2003. Nitrogen fixation in bryophytes, lichens, and decaying wood along a soil-age gradient in Hawaiian Montane Rain Forest. Biotropica 35:12-19.
48. Mayr, C., G. Försterra, V. Häussermann, A. Wunderlich, J. Grau, M. Zieringer, et al. 2011. Stable isotope variability in a Chilean food-web: Implications for N- and C-cycles. Mar. Ecol. Prog. Ser. 428:89-104. doi: 10.3354/meps09015
49. Moore, H. 1977. The isotopic composition of ammonia, nitrogen dioxide and nitrate in the atmosphere. Atmos. Environ. 11:1239-1243.
50. 15N natural abundances and N use by tundra plants. Oecologia 107:386-394.
51. Nash, T. H. 2008. Nitrogen, its metabolism and potential contribution to ecosystems. Pp. 216-233 in T. H. Nash III, ed. Lichen biology. 2nd ed. Cambridge Univ. Press, Cambridge, U.K.
52. Palmqvist, K. 2000. Tansley Review No. 117 - carbon economy in lichens. New Phytol. 148:11-36.
53. Palmqvist, K., D. Campbell, A. Ekblad, and H. Johansson. 1998. Photosynthetic capacity in relation to nitrogen content and its partitioning in lichens with different photobionts. Plant Cell Environ. 21:361-372.
54. Palmqvist, K., L. Dahlman, F. Valladares, A. Tehler, L. G. Sancho, and J.E. Mattsson. 2002. CO2 exchange and thallus nitrogen across 75 contrasting lichen associations from different climate zones. Oecologia 133:295-306.
55. Pataki, D. E., J. R. Ehleringer, L. B. Flanagan, D. Yakir, D. R. Bowling, C. J. Still, et al. 2003. The application and interpretation of Keeling plots in terrestrial carbon cycle research. Global Biogeochem. Cycles 17:1022. doi: 10.1029/2001GB001850
56. Pavlova, E. A., and A. I. Maslov. 2008. Nitrate uptake by isolated bionts of the lichen Parmelia sulcata. Russ. J. Plant Physiol. 55:475-479.
57. Phillips, D. L., and P. L. Koch. 2002. Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114-125.
58. Posada, D. 2006. ModelTest Server: A web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Res. 34:W700-W703. doi: 10.1093/nar/gkl042
59. Posada, D. 2008. jModelTest: Phylogenetic model averaging. Mol. Biol. Evol. 25:1253-1256.
60. Post, D. M. 2002. Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83:703-718.
61. Rai, A. N. 1988. Nitrogen metabolism. Pp. 201-237 in M. Galun, ed. CRC handbook of lichenology. Vol. I. CRC Press, Inc., Boca Raton, FL.
62. 2 incorporation and metabolism in the lichen Peltigera aphthosa Willd. Planta 152:544-552.
63. Rai, A. N., P. Rowell, and W. D. P. Stewart. 1983. Mycobiont-cyanobiont interactions during dark nitrogen fixation by the lichen Peltigera aphtosa. Physiol. Plant. 57:285-290.
64. Richardson, D. H. S. 1999. War in the world of lichens: Parasitism and symbiosis as exemplified by lichens and lichenicolous fungi. Mycol. Res. 103:641-650.
65. Richardson, D. H. S., and D. C. Smith. 1968. Lichen physiology. IX. Carbohydrate movement from the Trebouxia symbiont of Xanthoria aureola to the fungus. New Phytol. 67:61-68.
66. 15N comparisons among different co-occurring lichen species from littoral rocky substrata. Lichenologist 37:93-95.
67. 15N as an integrator of the nitrogen cycle. Trends Ecol. Evol. 16:153-162.
68. Swofford, D. L. 2000. PAUP: phylogenetic analysis using parsimony (and other methods), Version 4. Sinauer Associates, Sunderland, MA.
69. Tozer, W. C., D. Hackell, D. B. Miers, and W. B. Silvester. 2005. Extreme isotopic depletion of nitrogen in New Zealand lithophytes and epiphytes: The result of diffuse uptake of atmospheric ammonia? Oecologia 144:628-635.
70. 2-fixing plants from selected ecosystems. Oecologia 54:317-325.
71. Wang, Y. M., and M. J. Wooller. 2006. The stable isotopic (C and N) composition of modern plants and lichens from northern Iceland: With ecological and paleoenvironmental implications. Jökull 56:27-38.
72. Wiseman, R. D., and M. A. Wadleigh. 2002. Lichen response to changes in atmospheric sulphur: Isotopic evidence. Environ. Pollut. 116:235-241.