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

Abstract

Ramalina farinacea is an epiphytic fruticose lichen that is relatively abundant in areas with Mediterranean, subtropical or temperate climates. Little is known about photobiont diversity in different lichen populations. The present study examines the phycobiont composition of several geographically distant populations of R. farinacea from the Iberian Peninsula, Canary Islands and California as well as the physiological performance of isolated phycobionts. Based on anatomical observations and molecular analyses, the coexistence of two different taxa of Trebouxia (working names, TR1 and TR9) was determined within each thallus of R. farinacea in all of the analysed populations. Examination of the effects of temperature and light on growth and photosynthesis indicated a superior performance of TR9 under relatively high temperatures and irradiances while TR1 thrived at moderate temperature and irradiance. Ramalina farinacea thalli apparently represent a specific and selective form of symbiotic association involving the same two Trebouxia phycobionts. Strict preservation of this pattern of algal coexistence is likely favoured by the different and probably complementary ecophysiological responses of each phycobiont, thus facilitating the proliferation of this lichen in a wide range of habitats and geographic areas. © 2010 Society for Applied Microbiology and Blackwell Publishing Ltd.This study was funded by the Spanish Ministry of Education and Science (CGL2006-12917-C02-01/02), the Spanish Ministry of Science and Innovation (CGL2009-13429-C02-01/02), the AECID (PCI_A/024755/09) and the Generalitat Valenciana (PROMETEO 174/2008 GVA). We are grateful to Dr J. Gimeno-Romeu (University of California, Davis, USA) and to Dr P. J. G. de Nova (IREC, Ciudad Real, Spain), who were the first to isolate DNA from Ramalina farinacea thalli in our group. Wendy Ran revised the manuscript in English.Casano, L.; Del Campo, E.; García Breijo, FJ.; Reig Armiñana, J.; Gasulla, F.; Del Hoyo, A.; Guéra, A.... (2011). Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus Competition. Environmental Microbiology. 13(3):806-818. https://doi.org/10.1111/j.1462-2920.2010.02386.xS806818133Angert, A. L., Huxman, T. E., Chesson, P., & Venable, D. L. (2009). Functional tradeoffs determine species coexistence via the storage effect. Proceedings of the National Academy of Sciences, 106(28), 11641-11645. doi:10.1073/pnas.0904512106Baker, N. R., & Oxborough, K. (s. f.). Chlorophyll Fluorescence as a Probe of Photosynthetic Productivity. Advances in Photosynthesis and Respiration, 65-82. doi:10.1007/978-1-4020-3218-9_3Barreno , E. Herrera-Campos , M. García-Breijo , F. Gasulla , F. Reig-Armiñana , J. 2008 Non photosynthetic bacteria associated to cortical structures on Ramalina and Usnea thalli from Mexico http://192.104.39.110/archive/IAL6abstracts.pdfBECK, A., FRIEDL, T., & RAMBOLD, G. (1998). Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytologist, 139(4), 709-720. doi:10.1046/j.1469-8137.1998.00231.xBilger, W., & Bj�rkman, O. (1991). Temperature dependence of violaxanthin de-epoxidation and non-photochemical fluorescence quenching in intact leaves ofGossypium hirsutum L. andMalva parviflora L. Planta, 184(2), 226-234. doi:10.1007/bf01102422Bj�rkman, O., & Demmig, B. (1987). Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta, 170(4), 489-504. doi:10.1007/bf00402983Bold, H. C., & Parker, B. C. (1962). Some supplementary attributes in the classification of chlorococcum species. Archiv f�r Mikrobiologie, 42(3), 267-288. doi:10.1007/bf00422045Cenis, J. L. (1992). Rapid extraction of fungal DNA for PCR amplification. Nucleic Acids Research, 20(9), 2380-2380. doi:10.1093/nar/20.9.2380Del Campo, E. M., Casano, L. M., Gasulla, F., & 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. Molecular Phylogenetics and Evolution, 54(2), 437-444. doi:10.1016/j.ympev.2009.10.024Demmig-Adams, B., & Adams, W. W. (1996). The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science, 1(1), 21-26. doi:10.1016/s1360-1385(96)80019-7Demmig-Adams, B., M�guas, C., Adams, W. W., Meyer, A., Kilian, E., & 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(3), 400-409. doi:10.1007/bf01160396DePriest, P. T. (2004). Early Molecular Investigations of Lichen-Forming Symbionts: 1986–2001. Annual Review of Microbiology, 58(1), 273-301. doi:10.1146/annurev.micro.58.030603.123730DOERING, M., & PIERCEY-NORMORE, M. D. (2009). Genetically divergent algae shape an epiphytic lichen community on Jack Pine in Manitoba. The Lichenologist, 41(1), 69-80. doi:10.1017/s0024282909008111Friedl, T. (1989). Comparative ultrastructure of pyrenoids inTrebouxia (Microthamniales, Chlorophyta). Plant Systematics and Evolution, 164(1-4), 145-159. doi:10.1007/bf00940435Gasulla, F., de Nova, P. G., Esteban-Carrasco, A., Zapata, J. M., Barreno, E., & Guéra, A. (2009). Dehydration rate and time of desiccation affect recovery of the lichenic algae Trebouxia erici: alternative and classical protective mechanisms. Planta, 231(1), 195-208. doi:10.1007/s00425-009-1019-yGasulla, F., Guéra, A., & Barreno, E. (2010). “A simple and rapid method for isolating lichen photobionts“. Symbiosis, 51(2), 175-179. doi:10.1007/s13199-010-0064-4Gauze, G. F. (1934). The struggle for existence, by G. F. Gause. doi:10.5962/bhl.title.4489Genty, 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 (BBA) - General Subjects, 990(1), 87-92. doi:10.1016/s0304-4165(89)80016-9Gross, K. (2008). Positive interactions among competitors can produce species-rich communities. Ecology Letters, 11(9), 929-936. doi:10.1111/j.1461-0248.2008.01204.xGUZOW-KRZEMIŃSKA, B. (2006). Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. The Lichenologist, 38(5), 469-476. doi:10.1017/s0024282906005068Haruta, S., Kato, S., Yamamoto, K., & Igarashi, Y. (2009). Intertwined interspecies relationships: approaches to untangle the microbial network. Environmental Microbiology, 11(12), 2963-2969. doi:10.1111/j.1462-2920.2009.01956.xJOHANSEN, S., & HAUGEN, P. (2001). A new nomenclature of group I introns in ribosomal DNA. RNA, 7(7), 935-936. doi:10.1017/s1355838201010500Jones, A. ., Berkelmans, R., van Oppen, M. J. ., Mieog, J. ., & Sinclair, W. (2008). A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society B: Biological Sciences, 275(1641), 1359-1365. doi:10.1098/rspb.2008.0069Kopecky, J., Azarkovich, M., Pfündel, E. E., Shuvalov, V. A., & Heber, U. (2005). Thermal Dissipation of Light Energy is Regulated Differently and by Different Mechanisms in Lichens and Higher Plants. Plant Biology, 7(2), 156-167. doi:10.1055/s-2005-837471Kosugi, M., Arita, M., Shizuma, R., Moriyama, Y., Kashino, Y., Koike, H., & Satoh, K. (2009). Responses to Desiccation Stress in Lichens are Different from Those in Their Photobionts. Plant and Cell Physiology, 50(4), 879-888. doi:10.1093/pcp/pcp043Kranner, I., Cram, W. J., Zorn, M., Wornik, S., Yoshimura, I., Stabentheiner, E., & Pfeifhofer, H. W. (2005). Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proceedings of the National Academy of Sciences, 102(8), 3141-3146. doi:10.1073/pnas.0407716102Kroken, S., & Taylor, J. W. (2000). Phylogenetic Species, Reproductive Mode, and Specificity of the Green AlgaTrebouxiaForming Lichens with the Fungal GenusLetharia. The Bryologist, 103(4), 645-660. doi:10.1639/0007-2745(2000)103[0645:psrmas]2.0.co;2Little, A. F. (2004). Flexibility in Algal Endosymbioses Shapes Growth in Reef Corals. Science, 304(5676), 1492-1494. doi:10.1126/science.1095733Loarie, S. R., Duffy, P. B., Hamilton, H., Asner, G. P., Field, C. B., & Ackerly, D. D. (2009). The velocity of climate change. Nature, 462(7276), 1052-1055. doi:10.1038/nature08649Muggia, L., Grube, M., & Tretiach, M. (2008). Genetic diversity and photobiont associations in selected taxa of the Tephromela atra group (Lecanorales, lichenised Ascomycota). Mycological Progress, 7(3), 147-160. doi:10.1007/s11557-008-0560-6Niyogi, K. K. (2004). Is PsbS the site of non-photochemical quenching in photosynthesis? Journal of Experimental Botany, 56(411), 375-382. doi:10.1093/jxb/eri056O’Brien, H. E., Miadlikowska, J., & Lutzoni, F. (2005). Assessing host specialization in symbiotic cyanobacteria associated with four closely related species of the lichen fungusPeltigera. European Journal of Phycology, 40(4), 363-378. doi:10.1080/09670260500342647Ohmura, Y., Kawachi, M., Kasai, F., Watanabe, M. M., & Takeshita, S. (2006). Genetic combinations of symbionts in a vegetatively reproducing lichen,Parmotrema tinctorum, based on ITS rDNA sequences. The Bryologist, 109(1), 43-59. doi:10.1639/0007-2745(2006)109[0043:gcosia]2.0.co;2Piercey-Normore, M. D. (2005). The lichen-forming ascomyceteEvernia mesomorphaassociates with multiple genotypes ofTrebouxia jamesii. New Phytologist, 169(2), 331-344. doi:10.1111/j.1469-8137.2005.01576.xPombert, J.-F., Lemieux, C., & Turmel, M. (2006). BMC Biology, 4(1), 3. doi:10.1186/1741-7007-4-3Rambold, G., Friedl, T., & Beck, A. (1998). Photobionts in Lichens: Possible Indicators of Phylogenetic Relationships? The Bryologist, 101(3), 392. doi:10.1639/0007-2745(1998)101[392:pilpio]2.0.co;2Romeike, J., Friedl, T., Helms, G., & Ott, S. (2002). Genetic Diversity of Algal and Fungal Partners in Four Species of Umbilicaria (Lichenized Ascomycetes) Along a Transect of the Antarctic Peninsula. Molecular Biology and Evolution, 19(8), 1209-1217. doi:10.1093/oxfordjournals.molbev.a004181Rosenberg, E., Sharon, G., & Zilber-Rosenberg, I. (2009). The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework. Environmental Microbiology, 11(12), 2959-2962. doi:10.1111/j.1462-2920.2009.01995.xSchreiber, U., Schliwa, U., & Bilger, W. (1986). Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research, 10(1-2), 51-62. doi:10.1007/bf00024185Skaloud, P., & Peksa, O. (2010). Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta). Molecular Phylogenetics and Evolution, 54(1), 36-46. doi:10.1016/j.ympev.2009.09.035Wegley, L., Edwards, R., Rodriguez-Brito, B., Liu, H., & Rohwer, F. (2007). Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environmental Microbiology, 9(11), 2707-2719. doi:10.1111/j.1462-2920.2007.01383.xWeis, E., & Berry, J. A. (1987). Quantum efficiency of Photosystem II in relation to ‘energy’-dependent quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 894(2), 198-208. doi:10.1016/0005-2728(87)90190-3Wornik, S., & Grube, M. (2009). Joint Dispersal Does Not Imply Maintenance of Partnerships in Lichen Symbioses. Microbial Ecology, 59(1), 150-157. doi:10.1007/s00248-009-9584-yYAHR, R., VILGALYS, R., & DEPRIEST, P. T. (2004). Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Molecular Ecology, 13(11), 3367-3378. doi:10.1111/j.1365-294x.2004.02350.xYahr, R., Vilgalys, R., & DePriest, P. T. (2006). Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytologist, 171(4), 847-860. doi:10.1111/j.1469-8137.2006.01792.xZoller, S. (2003). Slow algae, fast fungi: exceptionally high nucleotide substitution rate differences between lichenized fungi Omphalina and their symbiotic green algae Coccomyxa. Molecular Phylogenetics and Evolution, 29(3), 629-640. doi:10.1016/s1055-7903(03)00215-

    Similar works