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Extremely Low Genetic Diversity of Stigonema Associated with Stereocaulon in Eastern Canada

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Extremely Low Genetic Diversity of Stigonema Associated with Stereocaulon in Eastern Canada Extremely low genetic diversity of Stigonema associated with Stereocaulon in eastern Canada Authors: Lavoie, Camille, Renaudin, M., McMullin, R. Troy, Gagnon, J., Roy, C., et al. Source: The Bryologist, 123(2) : 188-203 Published By: The American Bryological and Lichenological Society URL: https://doi.org/10.1639/0007-2745-123.2.188 BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Complete website, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/terms-of-use. Usage of BioOne Complete content is strictly limited to personal, educational, and non - commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Downloaded From: https://bioone.org/journals/The-Bryologist on 24 May 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by Universite Laval Extremely low genetic diversity of Stigonema associated with Stereocaulon in eastern Canada Camille Lavoie1, M. Renaudin2, R. Troy McMullin3, J. Gagnon4, C. Roy5, M.-E. Beaulieu1, J. P. Bellenger2 and J. C. Villarreal1,5,6,7 1 Departement´ de Biologie, Universite´ Laval, Quebec,´ Quebec,´ G1V 0A6, Canada; 2 Centre Seve,` Departement´ de Chimie, Universite´ de Sherbrooke, Quebec,´ Sherbrooke, J1K 2R1, Canada; 3 Canadian Museum of Nature, Research and Collections, Ottawa, Ontario, K1P 6P4, Canada; 4 Direction des Parcs Nationaux, Ministere` des Forets,ˆ de la Faune et des Parcs, Quebec,´ Quebec,´ G1S 4X4; 5 Herbier Louis-Marie, Universite´ Laval, Quebec,´ Quebec,´ G1V 0A6, Canada; 6 Smithsonian Tropical Research Institute, Panama City, Panama ABSTRACT. Stigomena is a genus of cyanobacteria that is often the photobiont associated with the lichen genus Stereocaulon. To elucidate the evolutionary relationships between Stereocaulon and Stigonema and assess whether there is specificity or selectivity at the ecosystem or species levels, we performed phylogenetic analyses on specimens collected throughout Eastern Canada. We generated ITS sequences from the fungal component of the symbiosis and sequences from the operon rbcL-rbcX and the trnL intron from the cyanobacteria of seventy specimens of Stereocaulon. Our ITS results revealed that at least forty Stereocaulon specimens are in 16 distinct species clades (OTUs) and morphologically defined species tend to be paraphyletic. In addition, two genera of cyanobacteria, Stigonema and Nostoc, were detected among the samples and the former is the most common symbiont associated with Stereocaulon.We discovered that nearly invariable Stigonema sequences (rbcL-rbcX) occur across 2,000 km of sampling from temperate to arctic biomes. The lack of geographic structure or species-level specificity for Stigonema suggest a high co-dispersal capability of the cyanobacteria with the ascomycete and selectivity towards a small number of very similar Stigonema haplotypes across eastern Canada. KEYWORDS. Coevolution, nitrogen fixation, Nordic ecosystems, symbiosis, phylogenetic diversity, specificity. ^^^ Mutualistic symbiosis provides insights on physio- 2018). The frequency of the partnership, or logical, chemical and genomic interactions between selectivity, describes the extent and diversity of the partners (Spribille et al. 2016; Steinhauser et al. association and this characteristic helps to predict 2016) and is one of the most spectacular biological underlying ecological processes shaping the mutu- interactions evolutionarily and ecologically. In order alistic interaction. Even in specific co-evolutionary to understand the role of each symbiont (e.g., trade- systems, such as figs and wasps, it is possible to offs and benefits between the partners) it is observe partner switches (Machado et al. 2005). To important to assess patterns of association, espe- better understand the extent of specificity and cially selectivity and specificity (Yahr et al. 2004). selectivity, phylogenetics can be used, as typically Organisms with high specificity are those with done in lichens (e.g., O’Brien et al. 2005; Yahr et al. narrow requirements for symbiotic partners. An 2004) extreme example is the co-evolution of the cyano- Lichens are the symbiotic organisms or hol- bacterium Anabaena with the fern Azolla (Li et al. obionts ‘‘par excellence’’; they are composed of a 7 Corresponding author’s e-mail: primary fungus (typically an ascomycete) (Spribille [email protected] et al. 2016), numerous bacteria (Bates et al. 2011) DOI: 10.1639/0007-2745-123.2.188 and a photobiont (algae and/or cyanobacteria) that The Bryologist 123(2), pp. 188–203 Published online: May 20 2020 0007-2745/20/$1.75/0 Copyright Ó2020 by The American Bryological and Lichenological Society, Inc. Downloaded From: https://bioone.org/journals/The-Bryologist on 24 May 2020 Terms of Use: https://bioone.org/terms-of-use Access provided by Universite Laval Lavoie et al.: Low diversity of Stigonema photobionts in Stereocaulon 189 co-exist in a composite state morphologically unlike sum; Brodo et al. 2001; Kershaw 1978; Payette & any of its components. Lichens have historically Delwaide 2018). Stereocaulon species have a mutu- been the subject of intense studies in almost every alistic association with nitrogen-fixing bacteria aspect of their symbiotic life style (Nash 2008 for a within structures called cephalodia (i.e., Nostoc or review). Additionally, the patterns of specificity and Stigonema, Fig. 2C) (Huss-Danell 1977, 1979; selectivity of the green algae (e.g., Asterochloris, Kershaw 1978; Kytovita¨ & Crittenden 2002). Across Chloroidium, Trebouxia) have been addressed at fine the Canadian Shield, the potential contribution of scales (Beck et al. 2002; Yahr et al. 2004) and fixed N2 from these bacteria to nutrient-poor soils globally (Dal Grande et al. 2014; Singh et al. 2017; makes Stereocaulon an important genus in early to Vancurovaˇ ´ et al. 2018). late successional stages of lichen woodlands (Crit- Molecular studies on the diversity and selectivity tenden & Kershaw 1978; Kershaw 1978). of the cyanobacterial symbiont or cyanobionts Stereocaulon has a global distribution, with 30 (especially the polyphyletic Nostoc and Rhizonema) species in Eastern Canada and ca. 20 species in the have typically used two variable markers, the trnL province of Quebec (Fig. 1; Esslinger et al. 2016) intron (Juriado¨ et al. 2019; O’Brien et al. 2005; that need systematic revision (Vancurovaˇ ´ et al. Rikkinen et al. 2002) and the rbcL-rbcX operon 2018). In eastern Canada, species of Stereocaulon (O’Brien et al. 2005, 2013; Rudi et al. 1998). The few occur throughout temperate-deciduous forests, the global studies on lichen cyanobionts support high boreal biome, the taiga and the Arctic tundra local diversity with ecologically specialized myco- (Brodo et al. 2001; Lamb 1951). Stereocaulon bionts associated with very few cyanobacterial associates with few genera of green algae (e.g., phylotypes, while symbiotically generalist fungal Asterochloris, Chloroidium), some of which (e.g., species tend to colonize new environments and Asterochloris irregularis) have a wide distribution display more flexibility (Lucking¨ et al. 2009; Magain (Vancurovaˇ ´ et al. 2018). The typical morphology of et al. 2017; O’Brien et al. 2005, 2013; Wirtz et al. most Sterocaulon species is a crustose thallus, that 2003). disappears in most species and a secondary thallus In fact, studies on Nostoc in cyanolichens or ‘‘pseudopodetia,’’ which support secondary suggest that broadly distributed cyanobionts associ- ramifications called ‘‘phyllocladia.’’ The cephalodia ated with a fungus may have a low evolutionary rate occur externally (unlike other lichen species such as or efficient dispersal mechanisms (Magain et al. Lobaria pulmonaria and Nephroma arcticum) on the 2017; O’Brien et al. 2005, 2013; Ota´lora et al. 2010; pseudopodetia or primary thallus (e.g., brownish Wirtz et al. 2003) or be a part of lichen guilds in Stigonema; Fig. 2B). Historically, two types of bipartite lichens, in which unrelated fungal species cephalodia have been described in Stereocaulon in similar habitats share the same cyanobionts (Johnson 1938; Lamb 1951): the small spherical (Juriado¨ et al. 2019; Rikkinen et al. 2002). Nostoc type (less than 1 mm in diameter) and the sacculate specificity may also be explained by asexual vs. type with a clear stipe and well-developed hyphal sexual dispersal mechanisms: lichen species with cortex. In species with the spherical type (e.g., S. asexual propagules may be dispersing the cyanobac- paschale and S. tomentosum), a short stipe supports teria along with them or selecting the previously the colony and the hyphae are finely intertwined existing cyanobionts from established asexual taxa with the outermost external part of the cyanobacte- (Belinchon´ et al. 2015; Rikkinen et al. 2002). rial filaments. Also, at the base of the cephalodium, In boreal eastern North America, lichens form the connection between the fungus and cyanobac- an extensive ground layer defining the lichen teria is more evident
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