Abstract
Since ice-free areas in Antarctica are predicted to increase by up to 25% before the end of this century, lichens such as the genus Placopsis will be important colonizers of these newly available grounds and will still be present in later successional stages of the lichen community. The main symbionts of Placopsis species are examined for 56 specimens collected from the South Shetland Islands, Antarctica using molecular (fungal and algal nrITS, fungal RPB1, algal rbcL sequences) and morphological methods. The specimens were collected from soils with different deglaciation times. Eight uni-algal photobiont cultures were obtained and analysed from two specimens. Placopsis antarctica and P. contortuplicata proved to be monophyletic and are sister species, only the former producing vegetative diaspores (soredia). Both share the same photobiont pool and are lichenized with two closely related species, Stichococcus antarcticus and S. allas. Two haplotypes of S. antarcticus are restricted to areas deglaciated for more than 5000 years and the volcanic Deception Island indicating a shift in the photobionts of Placopsis in the course of the soil and lichen community development. These photobiont haplotypes exhibit different ecological preferences, possibly leading to adaptation of the symbiotic entity to changing environmental conditions.
Similar content being viewed by others
References
Ahmadjian V (2001) Trebouxia: reflections on a perplexing and controversial lichen photobiont. In: Seckbach J (ed) Symbiosis. Springer, Houten, pp 373–383
Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csâki F (eds) Second International Symposium on Information Theory. Akadémia Kiado, Budapest, pp 267–281
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Armstrong R (2011) The biology of the crustose lichen Rhizocarpon geographicum. Symbiosis 55:53–67. https://doi.org/10.1007/s13199-011-0147-x
Beck A (2002) Selektivität der Symbionten schwermetalltoleranter Flechten. PhD thesis, Ludwig-Maximilians-Universität München, Munich, ISBN: 3-9808102-0-8
Beck A, Koop H-U (2001) Analysis of the photobiont population in lichens using a single-cell manipulator. Symbiosis 31:57–67
Beck A, Mayr C (2012) Nitrogen and carbon isotope variability in the green-algal lichen Xanthoria parietina and their implications on mycobiont-photobiont interactions. Ecol Evol 2:3132–3144
Belnap J, Büdel B, Lange OL (2001) Biological soil crusts: characteristics and distribution. In: Belnap J, Lange OL (eds) Biological Soil Crusts: Structure, Function, and Management. Ecological Studies (Analysis and Synthesis), vol 150. Springer, Berlin
Birkenmajer K (1992) Volcanic succession at Deception Island, West Antarctica: a revised lithostratigraphic standard. Studia Geologica Polonica 101:27–82
Bohuslavová O, Macek P, Redcenko O, Láska K, Nedbalová L, Elster J (2018) Dispersal of lichens along a successional gradient after deglaciation of volcanic mesas on northern James Ross Island, Antarctic Peninsula. Polar Biol 41:2221–2232
Borchhardt N, Schiefelbein U, Abarca N, Boy J, Mikhai-lyuk T, Sipman HJM, Karsten U (2017) Diversity of algae and lichens in biological soil crusts of Ardley and King George islands, Antarctica. Antarct Sci 29:229–237
Boy J, Godoy R, Shibistova O, Boy D, McCulloch R, De La Fuente AA, Morales MA, Mikutta R, Guggenberger G (2016) Successional patterns along soil development gradients formed by glacier retreat in the Maritime Antarctic, King George Island. Rev Chil Hist Nat 89. https://doi.org/10.1186/s40693-016-0056-8
Breen K, Lévesque E (2008) The influence of biological soil crusts on soil characteristics along a High Arctic Glacier Fore-land, Nunavut, Canada. Arct Antarct Alp Res 40:287–297
Casano LM, Del Campo EM, García-Breijo FJ, Reig-Armiñana J, Gasulla F, Del Hoyo A, Guéra 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
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772
De los Ríos A, Raggio J, Pérez-Ortega S, Vivas M, Pintado A, Green TGA, Ascaso C, Sancho LG (2011) Anatomical, morphological and ecophysiological strategies in Placopsis pycnotheca (lichenized fungi, Ascomycota) allowing rapid colonization of recently deglaciated soils. Flora-Morphology, Distribution, Functional Ecology of Plants 206:857–864
De Wever A, Leliaert F, Verleyen E, Vanormelingen P, Van der Gucht K, Hodgson DA, Sabbe K, Vyverman W (2009) Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia. Proc R Soc Lond B Biol Sci 276:3591–3599
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 31:17353–17366
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Edgar RC (2016) UCHIME2: Improved chimera detection for amplicon sequences. https://doi.org/10.1101/074252
Engelen A, Convey P, Popa O, Ott S (2016) Lichen photobiont diversity and selectivity at the southern limit of the maritime Antarctic region (Coal Nunatak, Alexander Island). Polar Biol 39:2403–2410
Ettl H, Gärtner G (2014) Syllabus der Boden-, Luft- und Flechtenalgen. Springer, Berlin
Favero-Longo SE, Worland MR, Convey P, Lewis-Smith RI, Piervittori R, Guglielmin M, Cannone N (2012) Primary succession of lichen and bryophyte communities following glacial recession on Signy Island, South Orkney Islands, Maritime Antarctic. Antarct Sci 24:323–336
Fermani P, Mataloni G, Van de Vijver B (2007) Soil microalgal communities on an Antarctic active volcano (Deception Island, South Shetlands). Polar Biol 30:1381–1393
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
Frey B, Bühler L, Schmutz S, Zumsteg A, Furrer G (2013) Molecular characterization of phototrophic microorganisms in the forefield of a receding glacier in the Swiss Alps. Environ Res Lett 8:015033
Fourcade NH (1972) Vulcanismo de la Isla Decepción. Contribución Del Instituto Antartico Argentino 148:1–18
Galloway DJ, Lewis-Smith RI, Quilhot W (2005) A new species of Placopsis (Agyriaceae: Ascomycota) from Antarctica. Lichenologist 37:321–327
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
Haugland JE, Beatty SW (2005) Vegetation establishment, succession and microsite frost disturbance on glacier forelands within patterned ground chronosequences. J Biogeogr 32:145–153
Hertel H (1988) Problems in monographing Antarctic crustose lichens. Polarforschung 58:65–76
Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing the confidence in phylogenetic analysis. Syst Biol 42:182–192
Hjört C, Björck S, Ingólfsson O, Möller P (1998) Holocene deglaciation and climate history of the northern Antarctic Peninsula region: a discussion of correlations between the Southern and Northern Hemispheres. Ann Glaciol 27:110–112
Hodač L, Hallmann C, Spitzer K, Elster J, Faßhauer F, Brinkmann N, Lepka D, Diwan V, Friedl T (2016) Widespread green algae Chlorella and Stichococcus exhibit polar-temperate and tropical-temperate biogeography. FEMS Microbiol Ecol 92:fiw122
Jones TC, Hogg ID, Wilkins RJ, Green TGA (2013) Photobiont selectivity for lichens and evidence for a possible glacial refugium in the Ross Sea Region, Antarctica. Polar Biol 36:767–774
Khan N, Tuffin M, Stafford W, Cary C, Lacap DC, Pointing SB, Cowan D (2011) Hypolithic microbial communities of quartz rocks from Miers Valley, McMurdo Dry Valleys, Antarctica. Polar Biol 34:1657–1668
Kvíderová J, Lukavský J (2005) The comparison of ecological characteristics of Stichococcus (Chlorophyta) strains isolated from polar and temperate regions. Algol Stud 118:127–140
Lamb IM (1947) A monograph of the lichen genus Placopsis Nyl. Lilloa 13:151–288
Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759
Leavitt SD, Kraichak E, Nelsen MP, Altermann S, Divakar PK, Alors D, Esslinger TL, Crespo A, Lumbsch HT (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
Lee JR, Raymond B, Bracegirdle TJ, Chadès I, Fuller RA, Shaw JD, Terauds A (2017) Climate change drives expansion of Antarctic ice-free habitat. Nature 547:49–54
Liu K, Warnow TJ, Holder MT, Nelesen SM, Yu J, Stamatakis AP, Linder CR (2012) SATe-II: very fast and accurate simultaneous estimation of multiple sequence alignments and phylogenetic trees. Syst Biol 61:90–106
López-Martínez J, Serrano E (2002) Geomorphology. In: López-Martínez J, Smellie JL, Thomson JW, Thomson MRA (eds) Geology and geomorphology of Deception Island. British Antarctic Survey. Natural Environment Research Council, Cambridge, pp 31–39
Mäusbacher R (1991) Die jungquartäre Relief- und Klimageschichte im Bereich der Fildeshalbinsel Süd-Shetland-Inseln, Antarktis. Heidelberger Geographische Arbeiten 89
Matheny PB, Liu YJ, Ammirati JF, Hall BD (2002) Using RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). Am J Bot 89:688–698
Medhaug I, Stolpe MB, Fischer EM, Knutti R (2017) Reconciling controversies about the ‘global warming hiatus’. Nature 545:41–47
Meredith MP, King JC (2005) Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys Res Lett 32:L19604
Michel RFM, Schaefer CEGR, López-Martínez J, Simas FNB, Haus NW, Serrano E, Bockheim JG (2014) Soils and landforms from Fildes Peninsula and Ardley Island, Maritime Antarctica. Geomorphology 225:76–86
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for Inference of Large Phylogenetic Trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, LA, U.S.A., pp 1–8
Mink S, López-Martínez J, Maestro A, Garrote J, Ortega JA, Serrano E, Durán JJ, Schmid T (2014) Insights into deglaciation of the largest ice-free area in the South Shetland Islands (Antarctica) from quantitative analysis of the drainage system. Geomorphology 225:4–24
Müller K, Müller J, Neinhuis C, Quandt D (2010) PhyDE: Phylogenetic Data Editor, version 0.9971, computer program [online], http://www.phyde.de
Muggia L, Leavitt S, Barreno E (2018) The hidden diversity of lichenized Trebouxiophyceae (Chlorophyta). Phycologia 57:503–524
Nascimbene J, Mayrhofer H, Dainese M, Bilovitz PO (2017) Assembly patterns of soil-dwelling lichens after glacier retreat in the European Alps. J Biogeogr 44:1393–1404
Nelsen MP, Rivas Plata E, Andrew CJ, Lücking R, Lumbsch HT (2011) Phylogenetic diversity of trentepohlialean algae associated with lichen-forming fungi. J Phycol 47:282–290
Neustupa J, Eliáš M, Šejnohová L (2007) A taxonomic study of two Stichococcus species (Trebouxiophyceae, Chlorophyta) with a starch-enveloped pyrenoid. Nova Hedwigia 84:51–63
Nolan C, Overpeck JO, Allen JRM, Anderson PM, Betancourt JL, Binney HA, Brewer S, Bush MB, Chase BM, Cheddadi R, Djamali M, Dodson J, Edwards ME, Gosling WD, Haberle S, Hotchkiss SC, Huntley B, Ivory SJ, Kershaw AP, Kin S-H, Latorre C, Leydet M, Lézine A-M, Liu K-B, Liu Y, Lozhkin AV, McGlone MS, Marchant RA, Momohara A, Moreno A, Müller S, Otto-Bliesner BL, Shen C, Stevenson J, Takahara H, Tarasov PE, Tipton J, Vincens A, Weng C, Xu Q, Zheng Z, Jackson ST (2018) Past and future global transformation of terrestrial ecosystems under climate change. Science 361:920–923
Ó Cofaigh C, Davies BJ, Livingstone SJ, Johnson JS, Smith JA, Anderson JB, Bentley MJ, Canals M, Domack E, Dowsdeswell JA, Evans J, Glasser NF, Hillenbrand C-D, Larter RD, Roberts SJ, Simms AR (2014) Reconstruction of ice-sheet changes in the Antarctic Peninsula since the Last Glacial Maximum. Quat Sci Rev 100:87–110
Olech M (2004) Lichens of King George Island, Antarctica. Drukarnia Uniwersytetu Jagiellńskiego, Kraków
Oliva M, Antoniades D, Giralt S, Granados I, Pla S, Toro M, Sanjurjo J, Liu EJ, Vieira G (2016) The Holocene deglaciation of the Byers Peninsula (Livingston Island, Antarctica) based on the dating of lake sedimentary records. Geomorphology 261:89–102
Olsacher J (1956) Contribución a la geología de la Antártida Occidental: I. Contribución al conocimiento geológico de la Isla Decepción. Contribución Del Instituto Antartico Argentino 2:1–76
Øvstedal D, Lewis-Smith R (2001) Lichens of Antarctica and South Georgia, A Guide to their identification and ecology. Cambridge University Press, Cambridge
Pattengale ND, Alipour M, Bininda-Emonds OR, Moret BM, Stamatakis A (2010) How many bootstrap replicates are necessary? J Comput Biol 17:337–354
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
Pérez-Ortega S, de los Ríos A, Crespo A, Sancho LG (2010) Symbiotic lifestyle and phylogenetic relationships of the bionts of Mastodia tessellata (Ascomycota, incertae sedis). Am J Bot 97:738–752
Pérez-Ortega S, Ortiz-Álvarez R, Green TGA, de los Ríos A (2012) Lichen myco- and photobiont diversity and their relationships at the edge of life (McMurdo Dry Valleys, Antarctica). FEMS Microbiol Ecol 82:429–448
Pessi IS, Pushkareva E, Lara Y, Borderie F, Wilmotte A, Elster J (2018) Marked succession of cyanobacterial communities following glacier retreat in the High Arctic. Microb Ecol. https://doi.org/10.1007/s00248-018-1203-3
Poelking EL, Schaefer CER, Fernandes Filho EI, de Andrade AM, Spielmann AA (2014) Soil-landform-plant communities relationships of a periglacial landscape at Potter Peninsula, Maritime Antarctica. Solid Earth Discussions 6:2261–2292
Posada D (2005) TCS 1.21 manual. Retrieved from: http://w3.ualg.pt/~rcastil/SOFTWARE_WINDOWS/TCS1.21/docs/TCS1.21.pdf
Pushkareva E, Pessi IS, Wilmotte A, Elster J (2015) Cyanobacterial community composition and impact of nutrient availability in Arctic soil crusts at different stages of development. FEMS Microbiol Ecol 91:fiv143. https://doi.org/10.1093/femsec/fiv143
Pushkareva E, Kvíderová J, Šimek M, Elster J (2017) Nitrogen fixation and diurnal changes of photosynthetic activity in Arctic soil crusts at different development state. Eur J Soil Biol 79:21–31
Raggio J, Green TGA, Crittenden PD, Pintado A, Vivas M, Pérez-Ortega S, de los Ríos A, Sancho LG (2012) Comparative ecophysiology of three Placopsis species, pioneer lichens in recently exposed Chilean glacial forelands. Symbiosis 56:55–66
Rindi F, Allali HA, Lam DW, López-Bautista JM (2010) An overview of the biodiversity and biogeography of terrestrial green algae. In: Rescigno V, Maletta S (eds) Biodiversity hotspots. Nova Science Publishers, Hauppauge, pp 105–122
Rippin M, Lange S, Sausen N, Becker B (2018) Biodiversity of biological soil crusts from the Polar Regions revealed by metabarcoding. FEMS Microbiol Ecol 94:fiy036
Rodriguez JM, Passo A, Chiapella JO (2018) Lichen species assemblage gradient in South Shetlands Islands, Antarctica: relationship to deglaciation and microsite conditions. Polar Biol 41:523–531
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 19:1209–1207
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Roy-Ocotla G, Carrera J (1993) Aeroalgae: response to some aerobiological questions. Grana 32:48–56
Ruprecht U, Brunauer G, Printzen C (2012) Genetic diversity of photobionts in Antarctic lecideoid lichens from an ecological view point. Lichenologist 44:661–678
Sancho LG, Schulz F, Schroeter B, Kappen L (1999) Bryophyte and lichen flora of South Bay (Livingston Island: South Shetland Islands, Antarctica). Nova Hedwigia 68:301–337
Schmidt SK, Reed SC, Nemergut DR, Grandy AS, Cleveland CC, Weintraub MN, Hill AW, Costello EK, Meyer AF, Neff JC et al (2008) The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently deglaciated soils. Proc R Soc B Biol Sci 275:2793–2802
Schmitt I, Lumbsch HT, Søchting U (2003) Phylogeny of the lichen genus Placopsis and its allies based on Bayesian analyses of nuclear and mitochondrial sequences. Mycologia 95:827–835
Seong YB, Owen LA, Lim HS, Yoon HI, Kim Y, Lee YI, Caffee MW (2009) Rate of late Quaternary ice-cap thinning on King George Island, South Shetland Islands, West Antarctica defined by cosmogenic 36Cl surface exposure dating. Boreas 38:207–213
Simões JC (2011) O papel do gelo antártico no sistema climático. In: Goldemberg J (ed) Antártica e as mudanḉas globais: um desafio para a humanidade 9. Blucher, São Paulo, pp 69–101
Simoes CL, da Rosa KK, Czapela FF, Vieira R, Simoes JC (2015) Collins Glacier Retreat Process and Regional Climatic Variations, King George Island, Antarctica. Geogr Rev 105:462–471
Soler-Membrives A, Linse K, Miller KJ, Arango CP (2017) Genetic signature of Last Glacial Maximum regional refugia in a circum-Antarctic sea spider. R Soc Open Sci 4:170615. https://doi.org/10.1098/rsos.170615
Spielmann AA, Pereira AB (2012) Lichens on the Maritime Antarctica. Glalia 4:1–28
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313
Stamatakis A (2016) The RAxML v8.2.X Manual. Heidelberg Institute for Theoretical Studies. http://sco.h-its.org/exelixis/web/software/raxml/#documentation. (5 June 2018, date last accessed)
Stamatakis A, Hoover P, Rougemont P (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771
Stiller JW, Hall BD (1997) The origin of red algae: implications for plastid evolution. Proc Natl Acad Sci U S A 94:4520–4525
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), Version 4 edn. Sinauer Associates, Sunderland
Thüs H, Muggia L, Pérez-Ortega S, Favero-Longo SE, Joneson S, O'Brien H, Nelsen MP, Duque-Thüs R, Grube M, Friedl T et al (2011) Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota). Eur J Phycol 46:399–415
Tibell L (2001) Photobiont association and molecular phylogeny of the lichen genus Chaenotheca. Bryologist 104:191–198
Tishkov RJ (1986) Primary succession in Arctic tundra on the west coast of Spitsbergen (Svalbard). Polar Geogr Geol 10:148–156
Turner J, Colwell SR, Marshall GJ, Lachlan-Cope TA, Carleton AM, Jones PD, Lagun V, Reid PA, Iagovkina S (2005) Antarctic climate change during the last 50 years. Int J Climatol 25:279–294
Turner J, Lu H, White I et al (2016) Absence of 21st century warming on Antarctic Peninsula consistent with natural variability. Nature 535:411–415
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Shinsky J, White T (eds) PCR Protocols: A Guide to Methods and Applications. Academic Press, London, pp 315–322
Wirtz N, Lumbsch HT, Green TGA, Türk R, Pintado A, Sancho L, Schroeter B (2003) Lichen fungi have low cyanobiont selectivity in maritime Antarctica. New Phytol 160:177–183
Zahradníková M, Andersen HL, Tønsberg T, Beck A (2018) Molecular evidence of Apatococcus, including A. fuscideae sp. nov., as photobiont in the genus Fuscidea. Protist 168:425–438
Zidarova R (2008) Algae from Livingston Island (S Shetland Islands): a checklist. Phytologia Balcanica 14:19–35
Acknowledgements
We cordially thank Dr. Georg Gärtner (Innsbruck, Austria) for providing the authentic culture of Stichococcus allas (ASIB: IB 37). Mark R. D. Seaward (Bradford, U. K.) is sincerely recognised for improving the English text.
Funding
The molecular part of this work was supported by the Staatliche Naturwissenschaftliche Sammlungen Bayerns [SNSBinnovativ to AB]. Logistic support was provided by the National Fund for Scientific and Technological Development [FONDECYT 1118745 to AC-K] and the Instituto Antártico Chileno [RT-2716 to AC-K].
Author information
Authors and Affiliations
Contributions
AB designed the study, collected the samples, isolated and analysed the photobiont cultures, guided the molecular work, prepared the photographs and wrote the manuscript. JB performed part of the molecular work, guided ID, did the phylogenetic analyses and wrote the manuscript. ACK provided logistic support and travel organization to Antarctica, participated in sample collection and revised the MS. ID performed part of the molecular work and revised the MS.
Corresponding author
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
(DOCX 48 kb)
ESM 2
(DOCX 27 kb)
ESM 3
(XLSX 24 kb)
Fig. S1
Phylogenetic relationships of Placopsis contortuplicata (PC) and P. antarctica (PA) photobionts and its allies. The phylogeny is based on ITS2 sequences and the topology shown here is the result of the Maximum Likelihood analysis. Bootstrap percentage values ≥70% are indicated at branches, followed by Shimodaira-Hasegawa values ≥0.70. Stars indicate Bayesian Posterior Probability values ≥0.95. AB-numbers refer to cultures. Stichococcus allas and S. antarcticus accessions are coloured according to their collection locality. Black letters indicate additional taxa from Antarctica. Abbreviations: Ar = Ardley, By = Byers Peninsula, Co = Coppermine Peninsula, DI = Deception Island, FI = Fildes Peninsula, KGI = King George Island, LI = Livingston Island, Po = Potter Peninsula, RI = Roberts Island; C = Centre, E = East, NE = Northeast, NW = Northwest, S = South, SE = Southeast, SW = Southwest, W = West. (PNG 699 kb)
Fig. S2
Green algal photobiont haplotype network based on rbcL sequences. AU = Austria Ötztal Alps, DI = Deception Island, KGI = King George Island, LI = Livingston Island, RI = Robert Island. (PNG 248 kb)
Fig. S3
Green algal photobiont haplotype network based on rbcL and ITS sequences. AU = Austria Ötztal Alps, CH = Switzerland Urner Alps, DI = Deception Island, KGI = King George Island, LI = Livingston Island, RI = Robert Island. (PNG 112 kb)
Rights and permissions
About this article
Cite this article
Beck, A., Bechteler, J., Casanova-Katny, A. et al. The pioneer lichen Placopsis in maritime Antarctica: Genetic diversity of their mycobionts and green algal symbionts, and their correlation with deglaciation time. Symbiosis 79, 1–24 (2019). https://doi.org/10.1007/s13199-019-00624-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-019-00624-4