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Assessing Host Specialization in Symbiotic Cyanobacteria Associated with Four Closely Related Species of the Lichen Fungus Peltigera

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Assessing Host Specialization in Symbiotic Cyanobacteria Associated with Four Closely Related Species of the Lichen Fungus Peltigera Eur. J. Phycol. (2005), 40: 363–378 Assessing host specialization in symbiotic cyanobacteria associated with four closely related species of the lichen fungus Peltigera HEATH E. O’BRIEN, JOLANTA MIADLIKOWSKA AND FRANC¸OIS LUTZONI Department of Biology, Duke University, Durham NC 27708, USA (Received 9 March 2005; accepted 31 August 2005) Heterocystous cyanobacteria form symbiotic associations with a wide range of plant and fungal hosts. We used a molecular phylogenetic approach to investigate the degree of host specialization of cyanobacteria associated with four closely related species of the lichenized fungus Peltigera, and to compare these strains with other symbiotic cyanobacteria. We conducted phylogenetic analyses on 16S, rbcLX, and trnL sequences from cyanobacteria associated with multiple specimens of each lichen species and from symbionts of other fungi and plants, as well as from free-living strains of Nostoc and related genera of cyanobacteria. The genus Nostoc comprises two divergent lineages, but symbiotic strains occur primarily within a single monophyletic lineage that also includes free-living representatives. Cyanobacteria from the same lichen species were often more closely related to strains from other species or to plant symbionts or free-living strains than to each other. These results indicate that host specialization is low for the genus Nostoc, and suggest that opportunities for coevolution with its partners may be rare. Key words: cyanobacteria, host association, lichens, molecular phylogenetics, Nostoc, Peltigera, specialization, specificity, symbiosis Introduction The cyanobacterial genus Nostoc presents an interesting case for studying host specialization Symbiotic associations are an important compo- because of the wide number of symbiotic associa- nent of the ecology of many cyanobacterial tions formed by members of the genus. In addition lineages and include interactions with plants to its role as a photosynthetic partner (photo- (Rai et al., 2000), fungi (Rai, 1990), animals biont) of a wide range of lichenized fungi (Wilkinson, 1992), and eukaryotic algae (Janson, (Tschermak-Woess, 1988), Nostoc also forms 2002; Murakami et al., 2004). It has been proposed symbiotic associations with a number of different that tightly integrated ecological associations, plants, including bryophytes (Adams, 2002), if maintained faithfully over evolutionary time- cycads (Costa & Lindblad, 2002), the flowering scales, can lead to coevolutionary patterns such plant Gunnera (Bergman, 2002), and possibly the as asymmetric evolutionary rates (Law & Lewis, fern Azolla (Plazinski et al., 1990; but see Peters 1983), gene-for-gene interactions (Flor, 1955) or & Meeks, 1989; Baker et al., 2003), as well as cospeciation (Brooks, 1979). Because coevolution the non-lichen fungus Geosiphon pyriforme (Kluge involves reciprocal evolutionary changes, it et al., 2002). Within lichens, Nostoc is thought to requires that each partner have a significant fitness be the sole photobiont occurring in most members effect on the other (Thompson, 1994). It has of the order Peltigerales sensu Miadlikowska been suggested that, if a species limits the number & Lutzoni (2004) and some members of of partners with which it interacts (specialization), the Lichinales (Tschermak-Woess, 1988) and this may increase the response of that species to Arctomiaceae (Lumbsch et al., 2005). It also selection imposed by those partners, facilitating occurs as a secondary photobiont in many green coevolution (Whitlock, 1996; Kawecki, 1998). algal lichens, including members of the Agyriaceae, Stereocaulaceae, and Peltigerales. Correspondence to: Heath O’Brien. Tel.: þ1 919 660-7382; It is not currently known if the same strains Fax: þ1 919 660-7293. e-mail: [email protected] of Nostoc are able to participate in these different ISSN 0967-0262 print/ISSN 1469-4433 online ß 2005 British Phycological Society DOI: 10.1080/09670260500342647 H. E. O’Brien et al. 364 associations or if Nostoc comprises multiple culture, it is difficult to ensure that the strains lineages that are each specialized on a different obtained do not represent minor symbionts or host. For most lichens, the evolutionary advan- epiphytes that grow faster than the primary tages of symbiont specialization must be balanced symbiont in culture (Meeks, 1998; Meeks et al., by the requirement for re-establishing the asso- 1988; Miao et al., 1997). ciation during each generation. While some lichen Molecular phylogenetic approaches can be used species have evolved specialized codispersal to overcome these difficulties by amplifying mechanisms such as soredia and isidia, which symbiont DNA directly from the host tissues and package together vegetative fungal hyphae and comparing them with axenically cultured reference photobiont cells (Bu¨del & Scheidegger, 1996), strains that have been examined morphologically many lichen fungi reproduce primarily through and physiologically. Sequence-based approaches sexually produced ascospores. These ascospores can also discriminate among morphologically disperse independently of the photobiont and indistinguishable strains, allowing examination of must reassociate with the cyanobacteria or algae fine-scale patterns of host-specialization among found in the immediate vicinity of the germinating closely related hosts. We used multi-locus phylo- ascospore. Specialization would reduce the number genetics to determine the extent of host specializa- of potential photobiont partners that germinating tion in Nostoc by comparing the relatedness spores are likely to encounter. Since the fungal of strains associated with the same host and partner is thought to be obligately symbiotic, those associated with different hosts. This was whereas free-living Nostoc is ubiquitous in many carried out at nested taxonomic scales: closely terrestrial habitats (Potts, 2000), evolutionary related species within the genus Peltigera section pressure toward specialization may differ for the Peltigera sensu Miadlikowska & Lutzoni (2000), two partners. Peltigera versus other cyanolichen genera, and Characterizing the degree of specialization in plants and other fungi versus lichenized fungi. cyanolichens has been hampered by problems In order to determine the taxonomic breadth of with cyanobacterial taxonomy, owing in large these symbiotic strains, we have also developed part to the lack of connection between studies a phylogenetic framework for heterocystous based on the botanical and bacteriological tradi- cyanobacteria by including sequences from tions (Turner, 1997). The former emphasizes well-studied reference strains representing six examination of freshly collected field material cyanobacterial genera. Specialization was and dried herbarium material (Geitler, 1932; examined for each partner by looking at the Koma´rek & Anagnostidis, 1989) while the latter amount of genetic diversity among cyanobacterial is based on examination of axenically cultured strains associating with the same host taxon reference strains, often with little information on and by looking at the taxonomic diversity the ecological distribution of the organisms of hosts associated with each cyanobacterial (Rippka et al., 1979; Castenholz, 2001). For lineage. example, the genus Nostoc was traditionally characterized by the formation of large gelatinous colonies (Koma´rek & Anagnostidis, 1989). Since Materials and methods this character is not exhibited in culture, bacter- iological treatments have defined Nostoc based on Taxon sampling the production of motile hormogonia (Rippka et Our taxon sampling is summarized in Table 1. al., 1979). However, hormogonia are not always We prepared two data sets: one to examine phylogenetic produced under standard cyanobacterial culture relationships among representative strains of different conditions and they have recently been reported genera within the Nostocales (dataset 1), and one to in cultures of Anabaena (Svenning et al., 2005). examine patterns of host specialization for symbiotic Likewise, species were traditionally recognized strains (dataset 2). Dataset 1 included 16S and rbcLX based on differences in colony morphology. It sequences of seven Nostoc strains (five environmental has been shown that these characters cannot be isolates and one cycad symbiont, as well as DNA used to diagnose monophyletic groups (Wright extracted directly from a colony of Nostoc commune et al., 2001), but no bacteriological species concept collected by HEO), three strains each of Anabaena, Aphanizomenon, and Nodularia, and one strain has been proposed for the group. These problems of Cylindrospermum, plus one strain of Fischerella are exacerbated in the case of symbiotic strains, (Stigonematales), for a total of 18 strains. because identification is usually based on micro- For examination of specialization (dataset 2), we scopic observation of symbiotic tissues, where the included 16S, rbcLX, and trnL. This necessitated morphology is often altered from the free-living obtaining trnL sequences for all the above strains state (Bergman & Ha¨llbom, 1982). Even in cases except the Aphanizomenon strains and two of where symbiotic cyanobacteria are isolated in pure the Anabaena strains, which were unavailable Cyanobacteria host specialization Table 1. Cyanobacterial strains used in this study with host or substrate information, location, collector and voucher information, and Genbank/EMBL accession numbers 16S rbcLX trnL Taxona Host/Substratea Location Voucher accession accession accession Dataset Nostoc
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