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Phylogenetic Diversity of the Lichenized Algal Genus Trebouxia (Trebouxiophyceae, Chlorophyta): a New Lineage and Novel Insights

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Phylogenetic Diversity of the Lichenized Algal Genus Trebouxia (Trebouxiophyceae, Chlorophyta): a New Lineage and Novel Insights applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Botanical Journal of the Linnean Society, 2020, XX, 1–9. With 3 figures. Downloaded from https://academic.oup.com/botlinnean/article-abstract/doi/10.1093/botlinnean/boaa050/5873858 by National and University Library of Iceland user on 05 August 2020 Phylogenetic diversity of the lichenized algal genus Trebouxia (Trebouxiophyceae, Chlorophyta): a new lineage and novel insights from fungal-algal association Keywords=Keywords=Keywords_First=Keywords patterns of Icelandic cetrarioid lichens (Parmeliaceae, HeadA=HeadB=HeadA=HeadB/HeadA Ascomycota) HeadB=HeadC=HeadB=HeadC/HeadB HeadC=HeadD=HeadC=HeadD/HeadC MAONIAN XU1, , HUGO DE BOER2, ELIN SOFFIA OLAFSDOTTIR1, Extract3=HeadA=Extract1=HeadA SESSELJA OMARSDOTTIR1 and STARRI HEIDMARSSON3,*, REV_HeadA=REV_HeadB=REV_HeadA=REV_HeadB/HeadA REV_HeadB=REV_HeadC=REV_HeadB=REV_HeadC/HeadB 1Faculty of Pharmaceutical Sciences, University of Iceland, Hagi, Hofsvallagata 53, IS-107 Reykjavik, REV_HeadC=REV_HeadD=REV_HeadC=REV_HeadD/HeadC Iceland 2Natural History Museum, University of Oslo, Sars’ gate 1, NO-0562 Oslo, Norway REV_Extract3=REV_HeadA=REV_Extract1=REV_HeadA 3Icelandic Institute of Natural History, Akureyri Division, IS-600 Akureyri, Iceland BOR_HeadA=BOR_HeadB=BOR_HeadA=BOR_HeadB/HeadA BOR_HeadB=BOR_HeadC=BOR_HeadB=BOR_HeadC/HeadB Received 3 June 2019; revised 20 March 2020; accepted for publication 11 June 2020 BOR_HeadC=BOR_HeadD=BOR_HeadC=BOR_HeadD/HeadC BOR_Extract3=BOR_HeadA=BOR_Extract1=BOR_HeadA EDI_HeadA=EDI_HeadB=EDI_HeadA=EDI_HeadB/HeadA Lichens have high tolerance to harsh environmental conditions, where lichen symbiont interactions (e.g. myco- and photobionts) may play a crucial role. The characterization of fungal-algal association patterns is essential to EDI_HeadB=EDI_HeadC=EDI_HeadB=EDI_HeadC/HeadB understand their symbiotic interactions. This study investigated fungal-algal association patterns in Icelandic EDI_HeadC=EDI_HeadD=EDI_HeadC=EDI_HeadD/HeadC cetrarioid lichens using a multi-locus phylogenetic framework, including fungal nrITS, MCM7, mtSSU, RPB1 and EDI_Extract3=EDI_HeadA=EDI_Extract1=EDI_HeadA RPB2 and algal nrITS, nrLSU, rbcL and mtCOXII data. Most Icelandic cetrarioid lichenized fungi were found to be specifically associated to the known Trebouxia clade “S” (Trebouxia simplex/suecica group), whereas the lichen- CORI_HeadA=CORI_HeadB=CORI_HeadA=CORI_HeadB/HeadA forming fungus Cetrariella delisei forms a symbiosis with a previously unrecognized lineage of Trebouxia, provisionally CORI_HeadB=CORI_HeadC=CORI_HeadB=CORI_HeadC/HeadB named as the “D” clade. This new Trebouxia lineage is supported by maximum likelihood and Bayesian phylogenetic CORI_HeadC=CORI_HeadD=CORI_HeadC=CORI_HeadD/HeadC analyses using all four included algal loci. CORI_Extract3=CORI_HeadA=CORI_Extract1=CORI_HeadA ADDITIONAL KEYWORDS: Iceland – lichen – Parmeliaceae – phylogeny – symbiosis – Trebouxia. ERR_HeadA=ERR_HeadB=ERR_HeadA=ERR_HeadB/HeadA ERR_HeadB=ERR_HeadC=ERR_HeadB=ERR_HeadC/HeadB ERR_HeadC=ERR_HeadD=ERR_HeadC=ERR_HeadD/HeadC INTRODUCTION whereas fungal specificity for photobionts represents specific or exclusive interactions between fungi and ERR_Extract3=ERR_HeadA=ERR_Extract1=ERR_HeadA Lichens are microbial communities, mainly consisting one certain type of photobiont (Singh et al., 2016). of nutritionally specialized heterotrophic fungi and INRE_HeadA=INRE_HeadB=INRE_HeadA=INRE_HeadB/HeadA The most common lichen photobionts are species in photosynthetic green algae and/or cyanobacteria INRE_HeadB=INRE_HeadC=INRE_HeadB=INRE_HeadC/HeadB the unicellular green algal genus Trebouxia Puymaly (Honegger, 1998). The photosynthetic partners are (Friedl & Rybalka, 2012). Species diversity of the INRE_HeadC=INRE_HeadD=INRE_HeadC=INRE_HeadD/HeadC called photobionts. Lichens exhibit high tolerance to genus is still poorly understood, as many Trebouxia INRE_Extract3=INRE_HeadA=INRE_Extract1=INRE_HeadA extreme environmental conditions, such as the polar spp. cannot be cultured using standard culture media, and desert regions, and they are the predominant life App_Head=App_HeadA=App_Head=App_HeadA/App_Head in turn leading to an underestimation of species forms on c. 8% of global land surface (Larson, 1987; BList1=SubBList1=BList1=SubBList diversity (Grube & Muggia, 2010). Furthermore, Domaschke et al., 2012). Environmental tolerance morphological characters from cultured Trebouxia BList1=SubBList3=BList1=SubBList2 and dispersal capability of lichens appears to be spp. have limited discriminatory power at the SubBList1=SubSubBList3=SubBList1=SubSubBList2 associated with the synergistic power of symbionts species or even genus level, as exemplified by six SubSubBList3=SubBList=SubSubBList=SubBList (De Vera, Rettberg & Ott, 2008). Fungal selectivity green algal species of Asterochloris Tschermak- for photobionts refers to their preferential selection of SubSubBList2=SubBList=SubSubBList=SubBList Woess that were mistakenly identified as Trebouxia photobionts when more than one photobiont is present, SubBList2=BList=SubBList=BList spp. using morphological characters (Skaloud & Peksa, 2010). Therefore, robust identification of *Corresponding author. E-mail: [email protected] those species relied on combining phylogenetic © 2020 The Linnean Society of London, Botanical Journal of the Linnean Society, 2020, XX, 1–9 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 2 M. XU ET AL. Downloaded from https://academic.oup.com/botlinnean/article-abstract/doi/10.1093/botlinnean/boaa050/5873858 by National and University Library of Iceland user on 05 August 2020 analysis with morphological evidence (Skaloud MATERIAL AND METHODS & Peksa, 2010). The algal nuclear ribosomal TAXON SAMPLING internal transcribed spacer region (algal nrITS) has been shown to be powerful in resolving species One hundred and sixty-eight specimens of Icelandic relationships in Trebouxia and uncovering the cetrarioid lichens from 13 species in six genera (Fig. 1) photobiont diversity in lichens (Kroken & Taylor, were sampled, including terricolous, epiphytic and 2000; Ruprecht, Brunauer & Printzen, 2012), and saxicolous taxa. The sampled terricolous taxa included it has been suggested that the algal nrITS region Cetraria aculeata (N = 11), Cetraria muricata (Ach.) should be used for DNA barcoding of Trebouxia spp. Eckfeldt (N = 14), Cetraria ericetorum Opiz (N = 8) due to its high genetic variability (Grube & Muggia, and Cetraria islandica (L.) Ach. (N = 54), with wide 2010; Friedl & Rybalka, 2012). Using available algal distributions in Iceland, and rarer species such as nrITS sequences in GenBank, phylogenetic analyses Cetrariella delisei (N = 26) and Flavocetraria nivalis (L.) have revealed that Trebouxia spp. tend to form Kärnefelt & A.Thell (N = 18) from southern Iceland and four well-supported monophyletic clades, including Flavocetraria cucullata (Bellardi) Kärnefelt & A.Thell clade “A” [Trebouxia arboricola Puymaly/ Trebouxia (N = 4) from near Lake Mývatn in northern Iceland. gigantea (Hildreth & Ahmadjian) Gärtner group], The sampled epiphytic lichen taxa included Cetraria clade “I” (Trebouxia impressa Ahmadjian/ Trebouxia sepincola (Ehrh.) Ach. (N = 6), with a wide distribution, gelatinosa Ahmadjian ex P.A.Archibald group), clade and Vulpicida pinastri (L.) J.-E.Mattsson & M.J.Lai (N “S” (Trebouxia simplex Tschermak-Woess/ Trebouxia = 3) and Tuckermannopsis chlorophylla (Willd.) Hale suecica Beck group) and clade “C” [Trebouxia corticola (N = 3) that are both most common in eastern Iceland. (P.A.Archibald) Gärtner/ Trebouxia galapagensis The sampled saxicolous lichen taxa included all three (Hildreth & Ahmadjian) Gärtner group] (Beck, 2002; species of Melanelia Essl., Melanelia hepatizon (Ach.) Helms, 2003; Leavitt et al., 2015). A.Thell (N = 10) with a wide distribution, and Melanelia Cetrarioid lichens are one of the most studied groups agnata (Nyl.) A.Thell (N = 7) and Melanelia stygia (L.) in the lichen-forming fungal family Parmeliaceae Essl. (N = 4) with more restricted distributions. Voucher (Nelsen et al., 2011). Morphologically they are information and GenBank accession numbers are characterized by erect foliose/subfruticose thalli with provided in Supporting Information (Table S1). marginal apothecia and pycnidia, and chemically they For the algal part of the study, the nrITS-based produce Cetraria Ach.-type lichenan polysaccharides reference operational taxonomic units (OTUs) delimited (Nelsen et al., 2011). Green algae associated with in Leavitt et al. (2015) were used as an initial framework cetrarioid lichen-forming fungi are exclusively from to identify our newly generated Trebouxia ITS sequences. Trebouxia (Honegger, 2009; Leavitt et al., 2015) The data matrix from Leavitt et al. (2015) encompasses Furthermore, Cetraria spp. specifically associate with the genetic diversity of Trebouxia algae from four known clade “S” Trebouxia (Leavitt et al., 2015). Several studies clades (“A”, “C”, “I” and “S”). The matrix was then further have focused on the cosmopolitan cetrarioid lichen enlarged to represent the whole genetic diversity of Cetraria aculeata (Schreb.) Fr. (Fernández-Mendoza Trebouxia by including additional reference sequences of et al.,
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