Skip to main content
SpringerLink
Log in

Amphitropical variation of the algal partners of Pseudephebe (Parmeliaceae, lichenized fungi)

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Lichens are present in most terrestrial ecosystems on Earth and colonize extreme habitats, where vascular plants are unable to thrive, due to unique properties of the fungal-algal symbiosis. Here, we explored the phylogeographic structure of green algae engaged in symbiosis with species in the genus Pseudephebe (Parmeliaceae). These often form deep brown to blackish fruticose thalli on acidic rocks, and have partially overlapping distributions: P. minuscula is bipolar and co-occurs with P. pubescens in Europe. Based on a broad sampling, including the Arctic and Antarctica, we focused on photobionts (1) to identify genetic lineages and their phylogenetic assignment, (2) to infer the haplotype distribution in relation with geography and the mycobiont’s identity, and (3) to evaluate spatial genetic structure and polymorphism. Results revealed three Trebouxia clade S lineages (Trebouxia S02, T. suecica and T. angustilobata) associated to Pseudephebe species, with predominant haplotypes distributed throughout the entire geographic distribution, and some, less frequent, shared between widely distant localities. Photobiont switching was evident in the Mediterranean region, and algal co-occurrence was frequent in both mycobionts, which shared the same set of photobionts; this could explain, at least partially, their overlapping distribution. Furthermore, genetic structure was influenced by geography given the substantial percentages of genetic variation (ca. 25–50%) explained by the different delimited eco−/biogeographic regions. In Continental Antarctica, mycobionts showed a high specialization towards the photobionts, which are probably endemic of this climatically extreme region. Taken together, our findings provide further insight about the processes shaping lichen biogeography.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available in GenBank (DNA sequences) and FigShare (alignments, https://doi.org/10.6084/m9.figshare.12587645), and the Pseudephebe thalli are kept in the following herbaria: the Royal Botanical Garden of Madrid (MA), University of Graz-Institute of Plant Sciences (GZU), Michigan State University (MSC), Herbario Nacional de Bolivia (LPB), University Complutense of Madrid-Faculty of Pharmacy (MAF), and University of Copenhagen (C).

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Álvarez R, del Hoyo A, Díaz-Rodríguez C, Coello AJ, del Campo EM, Barreno E, Catalá M, Casano LM (2015) Lichen rehydration in heavy metal-polluted environments: Pb modulates the oxidative response of both Ramalina farinacea thalli and its isolated microalgae. Microb Ecol 69:698–709

    Article  PubMed  CAS  Google Scholar 

  • Bačkor M, Peksa O, Škaloud P, Bačkorová M (2010) Photobiont diversity in lichens from metal-rich substrata based on ITS rDNA sequences. Ecotoxicol Environ Saf 73(4):603–612

    Article  PubMed  CAS  Google Scholar 

  • Barreno E, Pérez-Ortega S (2003) Líquenes de la Reserva Natural Integral de Muniellos, Asturias. Ed KRK, Oviedo

    Google Scholar 

  • Beck A, Friedl T, Rambold G (1998) Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytol 139:709–720

    Article  CAS  Google Scholar 

  • Blaha J, Baloch E, Grube M (2006) High photobiont diversity associated with the euryoecious lichen-forming ascomycete Lecanora rupicola (Lecanoraceae, Ascomycota). Biol J Linn Soc 88:283–293

    Article  Google Scholar 

  • Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9

    Article  PubMed  PubMed Central  Google Scholar 

  • Boluda CG, Hawksworth DL, Divakar PK, Crespo A, Rico VJ (2016) Microchemical and molecular investigations reveal Pseudephebe species as cryptic with an environmentally modified morphology. Lichenologist 48(5):527–543

    Article  Google Scholar 

  • Brodo IM, Sharnoff SD, Sharnoff S, Canadian Museum of Nature (2001) Lichens of North America. Yale University Press, New Haven

    Google Scholar 

  • Buschbom J, Mueller GM (2006) Testing “species pair” hypotheses: evolutionary processes in the lichen-forming species complex Porpidia flavocoerulescens and Porpidia melinodes. Mol Biol Evol 23(3):574–586

    Article  CAS  PubMed  Google Scholar 

  • Casano LM, del Campo EM, García-Breijo FJ, Reig-Armiñana J, Gasulla F, Del Hoyo A, Barreno E (2011) Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition? Environ Microbiol 13:806–818

    Article  CAS  PubMed  Google Scholar 

  • Castello M, Nimis PL (1997) Diversity of lichens in Antarctica. In: Battaglia B, Valencia J, Walton DWH (eds) Antarctic communities: species, structure and survival. Cambridge University Press, Cambridge, pp 15–21

    Google Scholar 

  • Català S, Del Campo EM, Barreno E, García-Breijo FJ, Reig-Armiñana J, Casano LM (2016) Coordinated ultrastructural and phylogenomic analyses shed light on the hidden phycobiont diversity of Trebouxia microalgae in Ramalina fraxinea. Mol Phylogenet Evol 94:765–777

    Article  PubMed  Google Scholar 

  • Chen JM, Werth S, Sork VL (2016) Comparison of phylogeographical structures of a lichen-forming fungus and its green algal photobiont in western North America. J Biogeogr 43(5):932–943

    Article  Google Scholar 

  • Dal Grande F, Rolshausen G, Divakar PK, Crespo A, Otte J, Schleuning M, Schmitt I (2018) Environment and host identity structure communities of green algal symbionts in lichens. New Phytol 217(1):277–289

    Article  CAS  PubMed  Google Scholar 

  • De los Ríos A, Ascaso C (2002) Preparative techniques for transmission electron microscopy and confocal laser scanning microscopy of lichens. In: Kranner I, Beckett RP, Varma AK (eds) Protocols in lichenology. Springer-Verlag, Berlin, Heidelberg, pp 87–117

    Chapter  Google Scholar 

  • Del Campo EM, Casano LM, Barreno E (2013) Evolutionary implications of intron-exon distribution and the properties and sequences of the RPL10A gene in eukaryotes. Mol Phylogenet Evol 66:857–867

    Article  PubMed  CAS  Google Scholar 

  • Devkota S, Chaudhary RP, Werth S, Scheidegger C (2019) Genetic diversity and structure of the epiphytic foliose lichen Lobaria pindarensis in the Himalayas depends on elevation. Fun Eco 41:245–255

    Article  Google Scholar 

  • Domaschke S, Fernández-Mendoza F, García MA, Martín M, Printzen C (2012) Low genetic diversity in Antarctic populations of the lichen-forming ascomycete Cetraria aculeata and its photobiont. Polar Res 31:17353

    Article  Google Scholar 

  • Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. Interaction 1:0.2413793

    Google Scholar 

  • Drenth A, McTaggart AR, Wingfield BD (2019) Fungal clones win the battle, but recombination wins the war. IMA Fungus 10:18

    Article  PubMed  PubMed Central  Google Scholar 

  • Du Rietz E (1940) Problems of bipolar plant distribution. Acta Phytogeogr Suec 13:215–282

    Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Fedrowitz K, Kaasalainen U, Rikkinen J (2012) Geographic mosaic of symbiont selectivity in a genus of epiphytic cyanolichens. Ecol Evol 2:2291–2303

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernández-Mendoza F, Printzen C (2013) Pleistocene expansion of the bipolar lichen Cetraria aculeata into the southern hemisphere. Mol Ecol 22:1961–1983

    Article  PubMed  Google Scholar 

  • Fernández-Mendoza F, Domaschke S, García MA, Jordan P, Martín MP, Printzen C (2011) Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol Ecol 20:1208–1232

    Article  PubMed  Google Scholar 

  • Friedl T (1989) Comparative ultrastructure of pyrenoids in Trebouxia (Microthamniales, Chlorophyta). Plant Syst Evol 164:145–159

    Article  Google Scholar 

  • Garrido-Benavent I, Pérez-Ortega S (2017) Past, present, and future research in bipolar lichen-forming fungi and their photobionts. Am J Bot 104(11):1660–1674

    Article  Google Scholar 

  • Garrido-Benavent I, Pérez-Ortega S, de los Ríos A (2017) From Alaska to Antarctica: species boundaries and genetic diversity of Prasiola (Trebouxiophyceae), a foliose chlorophyte associated with the bipolar lichen-forming fungus Mastodia tessellata. Mol Phylogenet Evol 107:117–131

  • Garrido-Benavent I, de los Ríos A, Fernández-Mendoza F, Pérez-Ortega S (2018) No need for stepping stones: direct, joint dispersal of the lichen-forming fungus Mastodia tessellata (Ascomycota) and its photobiont explains their bipolar distribution. J Biogeogr 45:213–224

    Article  Google Scholar 

  • Gasulla F, Guéra A, de los Ríos A, Pérez-Ortega S (2019) Differential responses to salt concentrations of lichen photobiont strains isolated from lichens occurring in different littoral zones. Plant Fungal Syst 64(2):149–162

  • Gilbert OL, Purvis OW (2009) Pseudephebe. In: Smith CW, Aptroot A, Coppins BJ, Fletcher A, Gilbert OL, James PW, Wolseley PA (eds) The lichens of Great Britain and Ireland. British Lichen Society, London, p 758

  • Hestmark G, Lutzoni F, Miadlikowska J (2016) Photobiont associations in co-occurring umbilicate lichens with contrasting modes of reproduction in coastal Norway. Lichenologist 48(5):545–557

    Article  Google Scholar 

  • Joly S, Stevens MI, van Vuuren BJ (2007) Haplotype networks can be misleading in the presence of missing data. Syst Biol 56:857–862

    Article  PubMed  Google Scholar 

  • Jukes T, Cantor C (1969) Evolution of protein molecules. In: Munro M (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Chapter  Google Scholar 

  • Katoh K, Misawa K, Kuma KI, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res 30:3059–3066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kroken S, Taylor JW (2000) Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist 103:645–660

    Article  CAS  Google Scholar 

  • Lamb IM (1948) Antarctic pyrenocarp lichens. Discov Rep 25:1–30

    Google Scholar 

  • Lamb IM (1970) Antarctic terrestrial plants and their ecology. In: Holdgate MW (ed) Antarctic ecology, 2nd edn. Academic Press, London, pp 733–751

    Google Scholar 

  • Leavitt SD, Kraichak E, Nelsen MP, Altermann S, Divakar PK, Alors D, Esslinger TL, Crespo A, Lumbsch T (2015) Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen-forming family Parmeliaceae (Ascomycota). Mol Ecol 24:3779–3797

    Article  PubMed  Google Scholar 

  • Leavitt SD, Kraichak E, Vondrak J, Nelsen MP, Sohrabi M, Pérez-Ortega S, St Clair LL, Lumbsch HT (2016) Cryptic diversity and symbiont interactions in rock-posy lichens. Mol Phylogenet Evol 99:261–274

    Article  PubMed  Google Scholar 

  • Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116

    Article  Google Scholar 

  • Letunic I, Bork P (2019) Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47:W256–W259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v. 5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lindblom L, Søchting U (2013) Genetic diversity of the photobiont of the bipolar lichen-forming ascomycete Xanthomendoza borealis. Herzogia 26:307–322

    Article  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the gateway computing environments workshop (GCE), pp 1–8 New Orleans

  • Molins A, Moya P, García-Breijo FJ, Reig-Armiñana J, Barreno E (2018) Molecular and morphological diversity of Trebouxia microalgae in sphaerothallioid Circinaria spp. lichens. J Phycol 54(4):494–504

    Article  PubMed  Google Scholar 

  • Muggia L, Pérez-Ortega S, Kopun T, Zellnig G, Grube M (2014) Photobiont selectivity leads to ecological tolerance and evolutionary divergence in a polymorphic complex of lichenized fungi. Ann Bot 114:463–475

    Article  PubMed  PubMed Central  Google Scholar 

  • Muggia L, Nelsen MP, Kirika PM, Barreno E, Beck A, Lindgren H, Lumbsch HT, Leavitt SD, Trebouxia working group. (2020) Formally described species woefully underrepresent phylogenetic diversity in the common lichen photobiont genus Trebouxia (Trebouxiophyceae, Chlorophyta): an impetus for developing an integrated taxonomy. Mol Phylogenet Evol 106821 https://doi.org/10.1016/j.ympev.2020.106821

  • Nadyeina O, Dymytrova L, Naumovych A, Postoyalkin S, Werth S, Cheenacharoen S, Scheidegger C (2014) Microclimatic differentiation of gene pools in the Lobaria pulmonaria symbiosis in a primeval forest landscape. Mol Ecol 23:5164–5178

    Article  CAS  PubMed  Google Scholar 

  • Nelsen MP, Gargas A (2008) Dissociation and horizontal transmission of codispersing lichen symbionts in the genus Lepraria (Lecanorales: Stereocaulaceae). New Phytol 177:264–275

    Article  CAS  PubMed  Google Scholar 

  • Nelsen MP, Gargas A (2009) Symbiont flexibility in Thamnolia vermicularis (Pertusariales: Icmadophilaceae). Bryologist 112(2):404–417

  • Nelsen MP, Lücking R, Boyce CK, Lumbsch HT, Ree RH (2020) No support for the emergence of lichens prior to the evolution of vascular plants. Geobiology 18(1):3–13

    Article  PubMed  Google Scholar 

  • Ohmura Y, Kawachi M, Kasai F, Watanabe MM, Takeshita S (2006) Genetic combinations of symbionts in a vegetatively reproducing lichen, Parmotrema tinctorum, based on ITS rDNA sequences. Bryologist 109:43–59

    Article  CAS  Google Scholar 

  • Ohmura Y, Takeshita S, Kawachi M (2019) Photobiont diversity within populations of a vegetatively reproducing lichen, Parmotrema tinctorum, can be generated by photobiont switching. Symbiosis 77:59–72

    Article  CAS  Google Scholar 

  • Onuţ-Brännström I, Tibell L, Johannesson H (2017) A worldwide phylogeography of the whiteworm lichens Thamnolia reveals three lineages with distinct habitats and evolutionary histories. Ecol Evo 7:3602–3615

    Article  Google Scholar 

  • Onuț-Brännström I, Benjamin M, Scofield DG, Heiðmarsson S, Andersson MG, Lindström ES, Johannesson H (2018) Sharing of photobionts in sympatric populations of Thamnolia and Cetraria lichens: evidence from high-throughput sequencing. Sci Rep 8(1):1–14

    Article  CAS  Google Scholar 

  • Opanowicz M, Grube M (2004) Photobiont genetic variation in Flavocetraria nivalis from Poland (Parmeliaceae, lichenized Ascomycota). Lichenologist 36(2):125–131

    Article  Google Scholar 

  • Ordynets A, Heilmann-Clausen J, Savchenko A, Bässler C, Volobuev S, Akulov O, Karadelev M, Kotiranta H, Saitta A, Langer E, Abrego N (2018) Do plant-based biogeographical regions shape aphyllophoroid fungal communities in Europe? J Biogeogr 45(5):1182–1195

    Article  Google Scholar 

  • Ortiz-Álvarez R, de los Ríos A, Fernández-Mendoza F, Torralba-Burrial A, Pérez-Ortega S (2015) Ecological specialization of two photobiont-specific maritime cyanolichen species of the genus Lichina. PLoS One 10:e0132718

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ossowska E, Guzow-Krzemińska B, Kolanowska M, Szczepańska K, Kukwa M (2019) Morphology and secondary chemistry in species recognition of Parmelia omphalodes group–evidence from molecular data with notes on the ecological niche modelling and genetic variability of photobionts. MycoKeys 61:39–74

    Article  PubMed  PubMed Central  Google Scholar 

  • Peat HJ, Clarke A, Convey P (2007) Diversity and biogeography of the Antarctic flora. J Biogeogr 34(1):132–146

    Article  Google Scholar 

  • Peksa O, Škaloud P (2011) Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Mol Ecol 20:3936–3948

    Article  PubMed  Google Scholar 

  • Pérez-Ortega S, Miller KA, de los Ríos A (2018) Challenging the lichen concept: Turgidosculum ulvae (Verrucariaceae) represents an independent photobiont shift to a multicellular blade-like alga. Lichenologist 50(3):341–356

  • Piercey-Normore MD, DePriest PT (2001) Algal switching among lichen symbioses. Am J Bot 88:1490–1498

    Article  CAS  PubMed  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17(1):208–212

  • Rikkinen J, Oksanen I, Lohtander K (2002) Lichen guilds share related cyanobacterial symbionts. Science 297:357

    Article  CAS  PubMed  Google Scholar 

  • Roca-Valiente B (2013) Estudio filogenético del grupo de “Rhizocarpon geographicum” (liquenes, Rhizocarpaceae, Ascomycota). Análisis contrastado de los caracteres morfológicos y los patrones biogeográficos. Universidad Complutense de Madrid, Madrid, Spain, Ph.D. dissertation

    Google Scholar 

  • Rolshausen G, Dal Grande F, Sadowska-Deś AD, Otte J, Schmitt I (2018) Quantifying the climatic niche of symbiont partners in a lichen symbiosis indicates mutualist-mediated niche expansions. Ecography 41:1380–1392

    Article  Google Scholar 

  • Rolshausen G, Hallman U, Grande FD, Otte J, Knudsen K, Schmitt I (2020) Expanding the mutualistic niche: parallel symbiont turnover along climatic gradients. P Roy Soc B-Biol SCI 287(1924):20192311

    Google Scholar 

  • Romeike 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. Mol Biol Evol 19:1209–1217

    Article  CAS  PubMed  Google Scholar 

  • Ruprecht U, Brunauer G, Printzen C (2012) Genetic diversity of photobionts in Antarctic lecideoid lichens from an ecological view point. Lichenologist 44:661–678

    Article  Google Scholar 

  • Sela I, Ashkenazy H, Katoh K, Pupko T (2015) GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res 43:W7–W14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seppelt RD (1995) Phytogeography of continental Antarctic lichens. Lichenologist 27:417–431

    Article  Google Scholar 

  • Singh G, Dal Grande F, Divakar PK, Otte J, Crespo A, Schmitt I (2017) Fungal-algal association patterns in lichen symbiosis linked to macroclimate. New Phytol 214:317–329

    Article  PubMed  Google Scholar 

  • Sork VL, Werth S (2014) Phylogeography of Ramalina menziesii, a widely distributed lichen-forming fungus in western North America. Mol Ecol 23(9):2326–2339

    Article  PubMed  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771

    Article  PubMed  Google Scholar 

  • Steinová J, Škaloud P, Yahr R, Bestová H, Muggia L (2019) Reproductive and dispersal strategies shape the diversity of mycobiont-photobiont association in Cladonia lichens. Mol Phylogenet Evol 134:226–237

    Article  PubMed  Google Scholar 

  • Stenroos S, Velmala S, Pykälä J, Ahti T (2016) Lichens of Finland. Norrlinia 30:1–896

    Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic association with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III Cladogram estimation Genetics 132:619–635

    CAS  PubMed  Google Scholar 

  • Thüs H, Muggia L, Pérez-Ortega S, Favero-Longo SE, Joneson S, O’Brien H, Nelsen MP, Duque-Thüs R, Grube M, Friedl T, Brodie J, Andrew CJ, Lücking R, Lutzoni F, Gueidan C (2011) Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota). Eur J Phycol 46(4):399–415

    Article  Google Scholar 

  • Vančurová L, Muggia L, Peksa O, Řídká T, Škaloud P (2018) The complexity of symbiotic interactions influences the ecological amplitude of the host: a case study in Stereocaulon (lichenized Ascomycota). Mol Ecol 27(14):3016–3033

    Article  PubMed  CAS  Google Scholar 

  • Vargas Castillo R, Beck A (2012) Photobiont selectivity and specificity in Caloplaca species in a fog-induced community in the Atacama Desert, northern Chile. Fungal Biol 116:665–676

    Article  PubMed  Google Scholar 

  • Werth S, Scheidegger C (2012) Congruent genetic structure in the lichen-forming fungus Lobaria pulmonaria and its green-algal photobiont. Mol Plant-Microbe Interact 25:220–230

    Article  CAS  PubMed  Google Scholar 

  • Werth S, Sork VL (2014) Ecological specialization in Trebouxia (Trebouxiophyceae) photobionts of Ramalina menziesii (Ramalinaceae) across six range-covering ecoregions of western North America. Am J Bot 101:1127–1140

    Article  PubMed  Google Scholar 

  • Woods AJ, Omernik JM, Pederson CL, Moran BC (2006) Level III and IV ecoregions of Illinois. EPA/600/R-06/104. USEPA National Health and environmental effects research lab., Corvallis, OR

  • Wornik S, Grube M (2010) Joint dispersal does not imply maintenance of partnerships in lichen symbioses. Microb Ecol 59(1):150–157

    Article  PubMed  Google Scholar 

  • Yahr R, Vilgalys R, DePriest PT (2006) Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytol 171:847–860

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Marine Technology Unit (UTM) of CSIC, and the Antarctica New Zealand agency for providing the necessary logistics for field work in Antarctica. We also thank Adam Flakus (Krakow, PL), Ana Millanes, Leopoldo G. Sancho and José Raggio (Madrid, ES), Antonio Gómez-Bolea and Esteve Llop (Barcelona, ES), Toby Spribille (Edmonton, CA), Ulrik Søchting (Copenhagen, DK) and Göran Thor (Uppsala, SE) for contributing to collections; Beatriz Martín Jouve (CNB, Madrid, ES) for her technical support in electron microscopy observation; Theodora Kopun (KFU Graz, AU) for her advice and help in the laboratory; and Helmut Mayrhofer and Martin Grube (KFU Graz, AU) for institutional support.

Funding

This study was financed by the Austrian FWF Einzelprojekt P26359 and partially by CTM2015–64728- C2–2-R (MINECO/FEDER, UE). IGB was supported by grant FPU AP2012–3556 (MECD) and “Estancia Breve-FPU” (no. EST14/00481, MECD), and SPO by RYC-2014-16,784 (MINECO).

Author information

Authors and Affiliations

  1. Department of Biogeochemistry and Microbial Ecology, National Museum of Natural Sciences (MNCN-CSIC), Serrano 115 dpdo, E-28045, Madrid, Spain

    Isaac Garrido-Benavent & Asunción de los Ríos

  2. Institute of Plant Sciences, Karl-Franzens-Universität Graz, A-8010, Graz, Austria

    Isaac Garrido-Benavent & Fernando Fernández-Mendoza

  3. Department of Mycology, Real Jardín Botánico (CSIC), Plaza Murillo 2, E-28014, Madrid, Spain

    Sergio Pérez-Ortega

Authors
  1. Isaac Garrido-Benavent
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sergio Pérez-Ortega
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Asunción de los Ríos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fernando Fernández-Mendoza
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analyses were performed by Isaac Garrido-Benavent, Sergio Pérez-Ortega, Asunción de los Ríos and Fernando Fernández-Mendoza. The first draft of the manuscript was written by Isaac Garrido-Benavent and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Isaac Garrido-Benavent.

Ethics declarations

Conflicts of interest/competing interests

Not applicable.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 102 kb)

ESM 2

(XLS 255 kb)

ESM 3

(XLSX 16 kb)

ESM 4

(PDF 140 kb)

ESM 5

(PDF 348 kb)

ESM 6

(PDF 83 kb)

ESM 7

(PDF 409 kb)

ESM 8

(PDF 273 kb)

ESM 9

(PDF 76 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Garrido-Benavent, I., Pérez-Ortega, S., de los Ríos, A. et al. Amphitropical variation of the algal partners of Pseudephebe (Parmeliaceae, lichenized fungi). Symbiosis 82, 35–48 (2020). https://doi.org/10.1007/s13199-020-00709-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-020-00709-5

Keywords

Search

Navigation