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Phylogenetic Studies of Cyanobacterial Lichens

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Phylogenetic Studies of Cyanobacterial Lichens Phylogenetic studies of cyanobacterial lichens Filip Högnabba Botanical Museum Finnish Museum of Natural History University of Helsinki Finland Plant Biology Department of Biological and Environmental Sciences University of Helsinki Finland Academic dissertation To be presented with the permission of the Faculty of Biosciences of the University of Helsinki for public criticism in Auditorium XII of the University Main Building, Unioninkatu 34, on March 30th 2007 at 12 o'clock noon. Helsinki 2007 © Filip Högnabba (summary, articles III, IV) © International Association for Plant Taxonomy (article I) © The British Mycological Society (article II) © The Willi Hennig Society (article V) Cover layout: Patrik Högnabba Author’s address: Botanical Museum P.O. Box 7 FI-00014 University of Helsinki Finland e-mail: [email protected] ISBN 978-952-92-1767-0 (paperback) ISBN 978-952-10-3798-6 (PDF) http://ethesis.helsinki.fi Yliopistopaino Helsinki 2007 Phylogenetic studies of cyanobacterial lichens Filip Högnabba This thesis is based on the following articles: I Myllys, L., Högnabba, F., Lohtander, K., Thell, A., Stenroos, S., Hyvönen, J. 2005. Phylogenetic relationships of Stereocaulaceae based on simultaneous analysis of beta-tubulin, GAPDH and SSU rDNA sequences. Taxon 54: 605- 618. II Högnabba, F. 2006. Molecular phylogeny of the genus Stereocaulon (Stereo- caulaceae, lichenized ascomycetes). Mycological Research 110: 1080-1092. III Högnabba, F., Stenroos, S., Thell, A., Myllys, L. Evolution of cyanobacterial symbioses in Ascomycota. Manuscript. IV Högnabba, F., Stenroos, S., Thell, A. Phylogenetic relationships and evolution of photobiont associations in Lobariaceae (Lecanoromycetes, Ascomycota). Manuscript. V Stenroos, S., Högnabba, F., Myllys, L., Hyvönen, J., Thell, A. 2006. High selectivity in symbiotic associations of lichenized ascomycetes and cyano- bacteria. Cladistics 22: 230-238. These are referred to in the text by the corresponding Roman numerals: Contributions The following table shows the major contributions of authors to the original articles or manuscripts. The initials refer to the authors of the articles in question. I II III IV V Original idea LM FH SS, FH FH, SS SS Data LM, FH FH SS, FH, AT FH, AT, SS FH, SS Analyses LM FH FH FH FH, SS Manuscript preparation LM, FH FH FH, SS FH SS, FH Supervised by: Doc. Soili Stenroos, Botanical Museum, Finnish Museum of Natural History, University of Helsinki Prof. Jaakko Hyvönen, Plant Biology, Department of Biological and Environmental Sciences, University of Helsinki Reviewed by: Dr. Harrie Sipman, Botanical Museum Berlin-Dahlem, Free University of Berlin, Germany Dr. Gunilla Ståhls-Mäkelä, Zoological Museum, Finnish Museum of Natural History, University of Helsinki Examined by: Prof. Anders Tehler, The Swedish Museum of Natural History, Stockholm, Sweden Summary Filip Högnabba Botanical Museum, P.O. Box 7, FI-00014 University of Helsinki, Finland. Introduction undergoes speciation. In modern classifications lichens are therefore treated as lichen-forming Lichens are intriguing mutualistic symbiotic fungi (Gargas et al., 1995; Honegger, 1996; assemblages between fungi (mycobiont) and Tehler, 1996). The lichen-forming life strategy green algae (phycobiont) or cyanobacteria has been adopted independently several times (cyanobiont) (see e.g. Honegger, 2001). during the evolutionary history of fungi (Gargas Associations including all three components in et al., 1995; James et al., 2006). Thus lichen- various combinations are also relatively forming fungi are not a monophyletic group. common (Hawksworth, 1988). Lichens are Lutzoni et al. (2001) show that lichenization therefore not organisms but can be viewed as may have occurred only once within the ecological phenomena or small ecosystems Ascomycota, but do not exclude the possibility (Tehler, 1996). Lichen symbiosis is a successful that this life strategy may have developed life strategy and lichens can be found in almost independently up to three times within the all terrestrial ecosystems, colonizing a wide Ascomycota. More importantly, Lutzoni et al. range of substrates. A few also occur in (2001) show that the symbiotic life strategy has freshwater and some are even found been lost repeatedly and that major fungal submerged in marine environments (Nash III, lineages are derived from lichen-forming 1996). Symbiosis between fungi and ancestors, a hypothesis also supported by autotrophic organisms, of which lichen Lutzoni et al. (2004). symbiosis is an example, has been suggested to At present about 13 500 fungal species be very old (Tehler, 1983; Tehler et al., 2003). have been recognized to be involved in lichen Recent fossil records support this view and it symbioses (Kirk et al., 2001). Of all lichen- has been shown that lichen-like symbioses forming species, 98% belong to the phylum were present 600 million years ago (Yuan et Ascomycota (Honegger, 1996). Of the al., 2005). approximately 32 000 species described in The taxonomy of lichen associations is Ascomycota, roughly 40% are lichen-forming based on the mycobiont, as this is the (Kirk et al., 2001). The majority of lichen component of the lichen that reproduces and symbioses (approximately 90%) are bipartite 5 associations between fungi and green algae, (Galloway, 1988; White & James, 1988). It has while about 10% are bipartite associations with been proposed to treat the cyanobacterial a cyanobacterium as the photobiont photomorphs as forma of the green algal (Tschermak-Woess, 1988). Tripartite species (Laundon, 1995), to give the associations, where green algae are more or cyanobacterial counterparts names without less evenly distributed in the lichen thallus nomenclatural status within quotation marks while cyanobacteria occur in specialized (Jørgensen, 1996), or to append “cyan.” or structures (cephalodia) spatially isolated from “chlor.” after the correct name (Heidmarsson, the green algae, occur in about 3-4% of lichens 1997). However, no consensus has been (Honegger, 1996). reached on this matter. One particular group of lichen-forming The main goal of my thesis was to fungi consists of species that are able to form reconstruct phylogenetic relationships of photomorphs, where the same fungal species defined groups of lichen-forming fungi that form symbioses with either green algae or include species involved in symbioses with cyanobacteria. The photomorphs may be cyanobacteria. Phylogenetic hypotheses morphologically very different, but representing natural relationships between morphologically similar photomorphs has also taxa should form the basis for classification. been demonstrated (James & Henssen, 1976). Based on phylogenetic relationships, the origin These photomorphs may occur separately or and evolution of specific symbioses, particularly form composite thalli (photosymbiodemes). those involving cyanaobacteria, were studied. The ability of lichen fungi to form Genetic diversity and phylogenetic photomorphs has resulted in taxonomical relationships of symbiotic cyanobionts were problems, particularly for those species in also studied in order to examine selectivity of which the photomorphs exist independently cyanobionts and mycobionts as well as possible (Laundon, 1995; Jørgensen, 1996, 1997, 1998; co-evolution between partners involved in Heidmarsson, 1997). It has been difficult to lichen associations. demonstrate that morphologically distinct The aims of study I were to examine the lichens contain the same fungus, and hence delimitation and position of Stereocaulaceae photomorphs of the same fungal species have based on multiple gene loci. In study II my at times been assigned to different genera. aims were to present a more detailed study of Careful morphological studies have, however, the phylogenetic relationships of the genus tied together morphologically different Stereocaulon (Stereocaulaceae) in order to test photomorphs (James & Henssen, 1976). The the existing infrageneric classification, to development of molecular tools has made the investigate the placement of some crustose recognition of photomorphs easier (Armaleo & species described in the genus, and to test the Clerc, 1991; Goffinet & Bayer, 1997; Stenroos suggested transfer of Muhria to Stereocaulon. et al., 2003; Takanashi et al., 2006a). According The aims of study III were to reconstruct the to the code of botanical nomenclature one phylogenetic relationships of Ascomycota and taxon can have only one correct name to examine the evolution of cyanobacterial (McNeill et al., 2006). However, different symbioses within the phylum. In study IV the names have often been assigned to different goals were to investigate the delimitation of photomorphs of the same fungal species the genera currently included in the family 6 Lobariaceae, to examine the relationships of of their simple morphology. Molecular markers previously poorly studied austral species, and can also be readily utilized in studies of co- finally to examine evolution and stability of evolution and specificity between mycobionts various symbiotic associations found within the and photobionts, even without identification of family. In study V genetic variation and the partners. phylogenetic relationships of cyanobionts were The phylogenetic analyses presented here examined and compared to those of free living are based solely on DNA sequence data. In cyanobacteria in order to study selectivity of studies I through IV the genetic diversity and mycobionts and photobionts involved in lichen phylogenetic relationships
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