Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus Competition?

Environmental Microbiology

Volumn 13, Issue 3, 2011, Pages 806-818

  Casano, Leonardo M ^a   Del Campo, Eva M ^a   García Breijo, Francisco J ^b,c   Reig Armiñana, José ^b   Gasulla, Francisco ^b   Del Hoyo, Alicia ^a   Guéra, Alfredo ^a,b   Barreno, Eva ^b  

^a UNIVERSITY OF ALCALÁ   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

^c UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ASCOMYCETES; CYTOLOGY; GREEN ALGA; LICHENS; LIGHT; PHOTOSYNTHESIS; PHYSIOLOGY; SPAIN; SYMBIOSIS; ULTRASTRUCTURE; UNITED STATES;

ASCOMYCOTA; CALIFORNIA; CHLOROPHYTA; LICHENS; LIGHT; PHOTOSYNTHESIS; SPAIN; SYMBIOSIS;

ALGAE; RAMALINA FARINACEA; TREBOUXIA;

EID: 79952089098     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02386.x     Document Type: Article

References (53)

1. Angert, A.L., Huxman, T.E., Chesson, P., and Venable, D.L. (2009) Functional tradeoffs determine species coexistence via the storage effect. Proc Nat Acad Sci USA 106: 11641-11645.
2. Baker, N.R., and Oxborough, K. (2004) Chlorophyll fluorescence as a probe of photosynthetic productivity. In Chlorophyll a Fluorescence: A Signature of Photosynthesis. Papageorgiou, G.C. (ed.). Dordrecht, The Netherlands: Springer, pp. 65-82.
3. Barreno, E. (2004) Hongos simbiontes: Líquenes, micoficobiosis y micorrizas. In Botánica. Izco, J. (ed.). Madrid, Spain: MacGraw-Hill Interamericana, pp. 309-340.
4. Barreno, E., Herrera-Campos, M., García-Breijo, F., Gasulla, F., and Reig-Armiñana, J. (2008) Non photosynthetic bacteria associated to cortical structures on Ramalina and Usnea thalli from Mexico. [WWW document]. URL Asilomar, Pacific Grove, CA, USA: Abstracts IAL 6- ABLS Joint Meeting, pp 5.
5. Beck, A., Friedl, T., and Rambold, G. (1998) Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytol 139: 709-720.
6. Bilger, W., and Björkman, O. (1991) Temperature dependence of violaxanthin deepoxidation and non-photochemical fluorescence quenching in intact leaves of Gossypium hirsutum L. and Malva parviflora L. Planta 184: 226-234.
7. Björkman, O., and Demmig, B. (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170: 489-504.
8. Bold, H.C., and Parker, B.C. (1962) Some supplementary attributes in the classification of Chlorococcum species. Arch Mikrobiol 42: 267-288.
9. Catalá, M., Gasulla, F., Pradas del Real, A., García-Breijo, F., Reig-Armiñana, J., and Barreno, E. (2010) Nitric oxide is involved in oxidative stress during rehydration of Ramalina farinacea (L.) Ach. in the presence of the oxidative air pollutant cumene hydroperoxide. In Bibliotheca Lichenologica 105 Nash, T. (ed.). Stuttgart, Germany: E. Schweizerbart Science Publishers, pp. 87-92.
10. Cenis, J.L. (1992) Rapid extraction of fungal DNA for PCR amplification. Nucleic Acids Res 20: 2380.
11. Del Campo, E.M., Casano, L.M., Gasulla, F., and Barreno, E. (2009) 23S rRNAs of lichen-forming trebouxia have multiple group I introns closely related to bacteria and fungi. Int Microbiol 12: 59-67.
12. Del Campo, E.M., Casano, L.M., Gasulla, F., and Barreno, E. (2010) Suitability of chloroplast LSU rDNA and its diverse group I introns for species recognition and phylogenetic analyses of lichen-forming Trebouxia algae. Mol Phylogenet Evol 54: 437-444.
13. Demmig-Adams, B., and Adams, W.W. III (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1: 21-26.
14. Demmig-Adams, B., Máguas, C., Adams, W.W. III, Meyer, A., Kilian, E., and Lange, O.L. (1990) Effect of high light on the efficiency of photochemical energy conversion in a variety of lichen species with green and blue-green phycobionts. Planta 180: 400-409.
15. DePriest, P.T. (2004) Early molecular investigations of lichen-forming symbionts: 1986-2001. Annu Rev Microbiol 58: 273-301.
16. Doering, M., and Piercey-Normore, M.D. (2009) Genetically divergent algae shape in epiphytic lichen community on jack pine in Manitoba. Lichenologist 41: 69-80.
17. Euzet, L., and Combes, C. (1980) Les problemes de l'especes chez les animaux parasites. In Les problemes de l'especes dans le regne animal. Bocquet, C., Génermont, J., and Lamotte, M. (eds). Paris, France: Societé Zoologique de France, pp. 239-285.
18. Friedl, T.H. (1989) Comparative ultrastructure of pyrenoids in Trebouxia (Microthamniales, Chlorophyta). Plant Syst Evol 164: 145-159.
19. Gasulla, F., de Nova, P.G., Esteban-Carrasco, A., Zapata, J.M., Barreno, E., and Guera, A. (2009) Dehydration rate and time of desiccation affect recovery of the lichen alga [corrected]Trebouxia erici: Alternative and classical protective mechanisms. Planta 231: 195-208.
20. Gasulla, F., Guéra, A., and Barreno, E. (2010) A simple micromethod for isolating lichen photobionts. Symbiosis 51: 175-179.
21. Gause, G.F. (1934) The Struggle For Existence. Baltimore, USA: Williams & Wilkins Co.
22. Genty, B., Briantais, J.M., and Baker, N.R. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87-92.
23. Gross, K. (2008) Positive interactions among competitors can produce species-rich communities. Ecol Lett 11: 929-936.
24. Grube, M., Cardinale, M., Vieira de Castro, J., Müller, H., and Berg, G. (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbiosis. Int Soc Microb Ecol J 3: 1105-1115.
25. Guzow-Krzeminska, B. (2006) Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. Lichenologist 38: 469-476.
26. Haruta, S., Kato, S., Yamamoto, K., and Igarashi, Y. (2009) Intertwined interspecies relationships: approaches to untangle the microbial network. Environ Microbiol 11: 2963-2969.
27. Honegger, R. (1991) Fungal evolution: symbiosis and morphogenesis. In Symbiosis as a Source of Evolutionary Innovation. Margulis, L., and Fester, R. (eds). Cambridge, MA, USA: The MIT Press, pp. 319-340.
28. Johansen, S., and Haugen, P. (2001) A new nomenclature of group I introns in ribosomal DNA. RNA 7: 935-936.
29. Jones, A.M., Berkelmans, R., van Oppen, M.J., Mieog, J.C., and Sinclair, W. (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc Biol Sci 275: 1359-1365.
30. Kopecky, J., Azarkovich, M., Pfundel, E.E., Shuvalov, V.A., and Heber, U. (2005) Thermal dissipation of light energy is regulated differently and by different mechanisms in lichens and higher plants. Plant Biol 7: 156-167.
31. Kosugi, M., Arita, M., Shizuma, R., Moriyama, Y., Kashino, Y., Koike, H., and Satoh, K. (2009) Responses to desiccation stress in lichens are different from those in their symbionts. Plant Cell Physiol 50: 879-888.
32. Kranner, I., Cram, W.J., Zorn, M., Wornik, S., Yoshimura, I., Stabentheiner, E., and Pfeifhofer, H.W. (2005) Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proc Nat Acad Sci USA 102: 3141-3146.
33. Kroken, S., and Taylor, J.W. (2000) Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist 103: 645-660.
34. Little, A.F., van Oppen, M.J., and Willis, B.L. (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304: 1492-1494.
35. Loarie, S.R., Duffy, P.B., Hamilton, H., Asner, G.P., Field, C.B., and Ackerly, D.D. (2009) The velocity of climate change. Nature 462: 1052-1055.
36. Muggia, L., Grube, M., and Tretiach, M. (2008) Genetic diversity and photobiont associations in selected taxa of the Tephromela atra group (Lecanorales, lichenised Ascomycota). Mycol Prog 7: 147-160.
37. Nelsen, M.P., and Gargas, A. (2008) Dissociation and horizontal transmission of codispersing lichen symbionts in the genus Lepraria (Lecanorales: Stereocaulaceae). New Phytol 177: 264-275.
38. Niyogi, K.K., Li, X.P., Rosenberg, V., and Jung, H.S. (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56: 375-382.
39. O'Brien, H., Miadlikowska, J., and Lutzoni, F. (2005) Assessing host specialization in symbiotic cyanobacteria associated with four closely related species of the lichen fungus Peltigera. Eur J Phycol 40: 363-378.
40. Ohmura, Y., Kawachi, M., Kasai, F., and Watanabe, M. (2006) Genetic combinations of symbionts in a vegetatively reproducing lichen, Parmotrema tinctorum, based on ITS rDNA sequences. Bryologist 109: 43-59.
41. Piercey-Normore, M.D. (2006) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii. New Phytol 169: 331-344.
42. Pombert, J.F., Lemieux, C., and Turmel, M. (2006) The complete chloroplast DNA sequence of the green alga Oltmannsiellopsis viridis reveals a distinctive quadripartite architecture in the chloroplast genome of early diverging Ulvophytes. BMC Biol 4: 3.
43. Rambold, G., Friedl, T., and Beck, A. (1998) Photobionts in lichens: Possible indicatorsof phylogenetic relationships? Bryologist 101: 392-397.
44. Romeike, J., Friedl, T., Helms, G., and Ott, S. (2002) Genetic diversity of algal and fungal partners in four species of Umbilicaria (lichenized ascomycetes) along a transect of the antarctic peninsula. Mol Biol Evol 19: 1209-1217.
45. Rosenberg, E., Sharon, G., and Zilber-Rosenberg, I. (2009) The hologenome theory of evolution contains Lamarckianaspects within a Darwinian framework. Environ Microbiol 11: 2959-2962.
46. Schreiber, U., Schliwa, U., and Bilger, W. (1986) Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10: 51-62.
47. Skaloud, P., and Peksa, O. (2010) Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta). Mol Phylogenet Evol 54: 36-46.
48. Wegley, L., Edwards, R., Rodriguez-Brito, B., Liu, H., and Rohwer, F. (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9: 2707-2719.
49. Weis, E., and Berry, J.A. (1987) Quantum efficiency of photosystem II in relation to 'energy'-dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta 894: 198-208.
50. Wornik, S., and Grube, M. (2009) Joint dispersal does not imply maintainance of partnerships in lichen symbioses. Microb Ecol 59: 150-157.
51. Yahr, R., Vilgalys, R., and Depriest, P.T. (2004) Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Mol Ecol 13: 3367-3378.
52. Yahr, R., Vilgalys, R., and DePriest, P.T. (2006) Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytol 171: 847-860.
53. Zoller, S., and Lutzoni, F. (2003) Slow algae, fast fungi: Exceptionally high nucleotide substitution rate differences between lichenized fungi Omphalina and their symbiotic green algae Coccomyxa. Mol Phylogenet Evol 29: 629-640.