Abstract
This study was focused on lichenicolous fungi from the Antarctic region whose diversity is not yet well known. The sampling was carried out in the maritime Antarctica, South Shetland Islands, Livingston Island, during a trip in 2018. In total, more than one hundred species of lichenicolous fungi were collected, of which a selection has been studied here. The remaining species will be studied in future papers. As a result of our morphological and molecular studies (based on ITS rDNA, LSU rDNA, and mtSSU), three new species are proposed: Arthonia olechiana on Steinera olechiana, Sphaeropezia neuropogonis on Usnea, and Sphinctrina sessilis on Pertusaria excludens. Moreover, the new combinations Bryostigma excentricum on Lepraria and Raesaenenia usneae on Usnea are also proposed.
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Data availability
All DNA sequences have been submitted to GenBank. The alignments can be downloaded from the supplementary material.
References
Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. https://doi.org/10.1093/nar/25.17.3389
Alstrup V, Elvebakk A (1996) Part 5. Fungi III. Lichenicolous fungi. In: Elvebakk A, Prestrud P (eds) A catalogue of Svalbard plants, fungi, algae and cyanobacteria, Norsk Plarinstitutt Skrifter, vol 198, pp 261–270
Alstrup V, Hawksworth DL (1990) The lichenicolous fungi of Greenland. Meddelelser om Gronland. Bioscience 31:1–90
Alstrup V, Olech M, Wietrzyk-Pelka P, Wegrzyn MH (2018) The lichenicolous fungi of the South Shetland Islands, Antarctica: species diversity and identification guide. Acta Soc Bot Pol 87:3607. https://doi.org/10.5586/asbp.3607
Baloch E, Gilenstam G Wedin M (2013) The relationships of Odontotrema (Odontotremataceae) and the resurrected Sphaeropezia (Stictidaceae)–new combinations and three new Sphaeropezia species. Mycologia 105:384–397. 10.3852/12–134
Bridge PD, Spooner BM (2012) Non-lichenized Antarctic fungi: transient visitors or members of a cryptic ecosystem? Fungal Ecol 5:381–394. https://doi.org/10.1016/j.funeco.2012.01.007
Cannon P, Ertz D, Frisch A, Aptroot A, Chambers S, Coppins B, Sanderson N, Simkin J, Wolselsey P (2020) Arthoniales: Arthoniaceae, including the genera Arthonia, Arthothelium, Briancoppinsia, Bryostigma, Coniocarpon, Diarthonis, Inoderma, Naevia, Pachnolepia, Reichlingia, Snippocia, Sporodophoron, Synarthonia and Tylophoron. Revisions of British and Irish Lichens 1:3–48. 10.34885/173
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Diederich P, Lawrey JD, Ertz D (2018) The 2018 classification and checklist of lichenicolous fungi, with 2000 non-lichenized, obligately lichenicolous taxa. The Bryologist 121:340–425. 10.1639/0007–2745–121.3.340
Diederich P, Zhurbenko M, Etayo J (2002) The lichenicolous species of Odontotrema (syn. Lethariicola) (Ascomycota, Ostropales). Lichenologist 34:479–501. https://doi.org/10.1006/lich.2002.0418
Divakar PK, Crespo A, Wedin M et al (2015) Evolution of complex symbiotic relationships in a morphologically derived family of lichen forming fungi. New Phytol 208:1217–1226. https://doi.org/10.1111/nph.13553
Divakar PK, Crespo A, Kraichak E, Leavitt SD, Singh G, Schmitt I, Lumbsch HT (2017) Using a temporal phylogenetic method to harmonize family-and genus-level classification in the largest clade of lichenforming fungi. Fungal Divers 84:101–117. https://doi.org/10.1007/s13225-017-0379-z
Dodge CW (1948) Lichens and lichen parasites. British and New Zealand Antarctic Research Expedition 1929–1931, Reports. Series B (Zoology and Botany) 7:1–276
Eriksson OE, Hawksworth DL (1989) Notes on ascomycete systematics—Nos. 804–888. Syst Ascomycetum 8:59–86
Ertz D, Tehler A (2011) The phylogeny of Arthoniales (Pezizomycotina) inferred from nucLSU and RPB2 sequences. Fungal Divers 49:47–71. https://doi.org/10.1007/s13225-010-0080-y
Ertz DR, Poulsen S, Charrier M, Søchting U (2017) Taxonomy and phylogeny of the genus Steinera (Arctomiales, Arctomiaceae) in the subantarctic islands of Crozet and Kerguelen. Phytotaxa 32:201–238. https://doi.org/10.11646/phytotaxa.324.3.1
Etayo J, Sancho LG (2006) Two lichenicolous ascomycetes on austral species of Usnea (Lecanorales, Ascomycota). Nova Hedwigia 83:483–488. https://doi.org/10.1127/0029-5035/2006/0083-0483
Etayo J, Sancho LG (2008) Hongos liquenícolas del Sur de Sudamérica, especialmente de Isla Navarino (Chile). Bibl Lichenol 98:1–302
Fries TM (1867) Lichenes Spitsbergenses determinavit T.H. Fries. Kongliga Svenska Vetenskaps-Akademiens Handlingar 7:1–53
Frisch A, Thor G, Ertz D, Grube M (2014) The arthonialean challenge: restructuring Arthoniaceae. Taxon 63:727–744. https://doi.org/10.12705/634.20
Frisch A, Holien H (2018) Arthonia toensbergii, a new lichenicolous fungus on Mycoblastus affinis from the boreal rainforests in Norway. Graph Scr 30:34–43
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomicetes. Application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Giavarini V, Purvis WO (2009) Sphinctrina. In: Smith CW, Aptroot A, Coppins BJ, Fletcher A, Gilbert OL, James PW, Wolseley PA (eds) The lichens of Great Britain and Ireland. The British Lichen Society, London, pp 847–848
Giraldo A, Gené J, Sutton DA, Wiederhold N, Guarro J (2017) New acremonium-like species in the Bionectriaceae and Plectosphaerellaceae. Mycol Progress 16:349–368. https://doi.org/10.1007/s11557-017-1271-7
Giraldo A, Gené J, Cano J, de Hoog S, Guarro J (2012) Two new species of Acremonium from Spanish soils. Mycologia 104:1456–1465. https://doi.org/10.3852/11-402
Giraldo A, Gené J, Cano J, de Hoog S, Decock C, Guarro J (2014) Acremonium with catenate elongate conidia: phylogeny of Acremonium fusidioides and related species. Mycologia 106:328–338. https://doi.org/10.3852/13-158
Glenn AE, Bacon CW, Price R, Hanlin RT (1996) Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 88:369–383. https://doi.org/10.1080/00275514.1996.12026664
Green TGA, Schroeter B, Sancho LG (2007) Plant life in Antarctica. In: Pugnaire FI, Valladares F (eds) Functional plant ecology, 2nd edn. Marcel Dekker Inc., New York, pp 389–433
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:95–98
Hawksworth DL (2003) The lichenicolous fungi of Great Britain and Ireland: an overview and annotated checklist. Lichenologist 35:191–232. https://doi.org/10.1016/S0024-2829(03)00027-6
Hawksworth DL, Iturriaga T (2006) Lichenicolous fungi described from Antarctica and the sub-Antarctic islands by Carroll W. Dodge (1895–1988). Antarctic Science 18:291–301. https://doi.org/10.1017/S0954102006000344
Hawksworth DL, Rossman AY (1997) Where are all the undescribed fungi? Phytopathol 87:888–891. https://doi.org/10.1094/PHYTO.1997.87.9.888
Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192. https://doi.org/10.1093/sysbio/42.2.182
Ihlen PG, Wedin M (2008) An annotated key to the lichenicolous Ascomycota (including mitosporic morphs) of Sweden. Nova Hedwigia 86:275–365. https://doi.org/10.1127/0029-5035/2008/0086-0275
Kondratyuk SY, Lőkös L, Halda J, Lee BG, Jang SH, Woo JJ, Park JS, Oh S-O, Han S-K Hur JS (2019) Arthonia dokdoensis and Rufoplaca toktoana–two new taxa from Dokdo Islands (South Korea). Mycobiology 47:355–367. https://doi.org/10.1080/12298093.2019.1688074
Kondratyuk SY, Upreti DK, Mishra GK, Nayaka S, Ingle KK, Orlov OO, Kondratyuk AS, Lokös L, Farkas E, Woo J-J, Hur JS (2020) New and noteworthy lichen-forming and lichenicolous fungi 10. Acta Bot Hung 62:69–108. https://doi.org/10.1556/034.62.2020.1-2.6
Lewis Smith RI (1984) Terrestrial plant biology of the Sub-Antarctic and Antarctic. In: LAWS RM (ed) Antarctic ecology. Academic Press, London, pp 61–162
Lindgren H, Diederich P, Goward T, Myllys L (2015) The phylogenetic analysis of fungi associated with lichenized ascomycete genus Bryoria reveals new lineages in the Tremellales including a new species Tremella huuskonenii hyperparasitic on Phacopsis huuskonenii. Fungal Biol 119:844–856. https://doi.org/10.1016/j.funbio.2015.06.005
Lücking R (2019) Stop the abuse of time! Strict temporal banding is not the future of rank-based classifications in fungi (including lichens) and other organisms. Crit Rev Plant Sci 38:199–253. https://doi.org/10.1080/07352689.2019.1650517
Lücking R, Hodkinson BP, Leavitt SD (2016) The 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota – approaching one thousand genera. Bryologist 119:361–416. https://doi.org/10.1639/0007-2745-119.4.361
Mayrhofer H (1987) Ergänzende Studien zur Taxonomie der Gattung Protothelenella. Herzogia 7:313–342
Miadlikowska J, Kauff F, Högnabba F et al (2014) A multigene phylogenetic synthesis for the class Lecanoromycetes (Ascomycota): 1307 fungi representing 1139 infrageneric taxa, 317 genera and 66 families. Mol Phylogenet Evol 79:132–168. https://doi.org/10.1016/j.ympev.2014.04.003
Miller MA, Pfeiffer W, Schwartz T (2010) The CIPRES science gateway. In: Proceedings of the Gateway Computing Environments Workshop (GCE):1–8.
Möller C, Gams W (1993) Two new hyphomycetes isolated from Antarctic lichens. Mycotaxon 48:441–450
Möller C, Dreyfuss MM (1996) Microfungi from Antarctic lichens, mosses and vascular plants. Mycologia 88:922–933. https://doi.org/10.1080/00275514.1996.12026732
Muñiz D, Llop E, Hladun NL (2013) Sphinctrina paramerae, a new Mediterranean lichenicolous species with non-septate spores. Lichenologist 45:137–143. https://doi.org/10.1017/S0024282912000801
Orange A, Purvis OW, James PW (2009) Protothelenella. In: Aptroot A, Coppins BJ, Fletcher A, Gilbert OL, James PW, Wolseley PA (eds) Smith CW. The lichens of Great Britain and Ireland. London, The British Lichen Society, pp 755–757
Øvstedal DO, Lewis Smith RI (2001) Lichens of Antarctica and South Georgia: a guide to their identification and ecology. Cambridge University Press, Cambridge
Øvstedal DO, Schaefer CEGR (2013) A new lichen species from the Heritage Range, Ellsworth Mountains, Antarctica. Hoehnea 40:361–364
Peat HJ, Clarke A, Convey P (2007) Diversity and biogeography of the Antarctic flora. Journal of Biogeography 34:132–146. https://doi.org/10.1111/j.1365-2699.2006.01565.x
Pérez-Ortega S, Garrido-Benavent I, De Los RA (2015) Austrostigmidium, a new austral genus of lichenicolous fungi close to rock-inhabiting meristematic fungi in Teratosphaeriaceae. Lichenologist 47:143–156. https://doi.org/10.1017/S0024282915000031
Peršoh D, Rambold G (2002) Phacopsis—a lichenicolous genus of the family Parmeliaceae. Mycol Prog 1:43–55. https://doi.org/10.1007/s11557-006-0004-0
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. https://doi.org/10.1093/molbev/msn083
Pino-Bodas R, Zhurbenko MP, Stenroos S (2017) Phylogenetic placement within Lecanoromycetes of lichenicolous fungi associated with Cladonia and some other genera. Persoonia 39:91–117. https://doi.org/10.3767/persoonia.2017.39.05
Prieto M, Baloch E, Tehler A, Wedin M (2013) Mazaedium evolution in the Ascomycota (Fungi) and the classification of mazaediate groups of formerly unclear relationship. Cladistics 29:296–308. https://doi.org/10.1111/j.1096-0031.2012.00429.x
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904. https://doi.org/10.1093/sysbio/syy032
Ronquist F, Teslenko M, Van der Mark P et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Rosa LH, Zani CL, Cantrell CL, Duke SO, Van Dijck P, Desideri A, Rosa CA (2019) Fungi in Antarctica: diversity, ecology, effects of climate change, and bioprospection for bioactive compounds. In: Rosa LH (ed) Fungi of Antarctica: diversity, ecology and biotechnological applications. Springer, Cham, pp 1–17. https://doi.org/10.1007/978-3-030-18367-7_1
Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S (2007) Fungi in Antarctica. Revi Environ Sci Biotechnol 6:127–141. https://doi.org/10.1007/s11157-006-9107-y
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
Sancho LG, Green TGA, Pintado A (2007) Slowest to fastest: extreme range in lichen growth rates supports their use as an indicator of climate change in Antarctica. Flora 202:667–673. https://doi.org/10.1016/j.flora.2007.05.005
Santesson R (1993) The lichens and lichenicolous fungi of Sweden and Norway. SBT-f¨orlaget, Lund
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge J L, Levesque CA, Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. PNAS 109:6241–6246. https://doi.org/10.1073/pnas.1117018109
Schmitt I, Del Prado R, Grube M et al (2009) Repeated evolution of closed fruiting bodies is linked to ascomata development in the largest group of lichenized fungi (Lecanoromycetes, Ascomycota). Mol Phylogenet Evol 52:34–44. https://doi.org/10.1016/j.ympev.2009.03.017
Stamatakis A, Ludwig T, Meier H (2005) RAxML-III: a fast program for maximum likelihood- based inference of large phylogenetic trees. Bioinform 21:456–463. https://doi.org/10.1093/bioinformatics/bti191
Summerbell RC, Gueidan C, Schroers HJ, de Hoog GS, Starink M, Arocha Rosete Y, Guarro J, Scott JA (2011) Acremonium phylogenetic overview and revision of Gliomastix, Sarocladium, and Trichothecium. Stud Mycol 68:139–162. https://doi.org/10.3114/sim.2011.68.06
Spegazzini C (1910) Mycetes Argentinenses 5. Anal Mus Nac Buenos Aires 20:329–467
Søchting U, Øvstedal DO, Sancho LG (2004) The lichens of Hurd peninsula, Livingston Island, south Shetlands, Antarctica. Bibl Lichenol 88:607–658
Terauds A, Lee JR (2016) Antarctic biogeography revisited: updating the Antarctic Conservation Biogeographic Regions. Divers Distrib 22:836–840. https://doi.org/10.1111/ddi.12453
Tibell L (2004) Sphinctrina. In Nash III, TH, Ryan BD, Diederich P, Gries C, Bungartz F. Licheno Flora of the Greater Sonoran Desert Region. Vo. 2. Lichens Unlimited, Arizona State University, Tempe, Arizona, pp 699–701.
Tibell L, Frisch A, Thor G (2014) Additions to the calicioid flora of Japan and Korea, with the descriptions of two new species. Ann Bot Fennici 51:189–194. https://doi.org/10.5735/085.053.0108
Triebel D, Rambold G (1988) Cecidonia und Phacopsis (Lecanorales): zwei lichenicole Pilzgattungen mit cecidogenen Arten. Nova Hedwigia 47:279–309
Triebel D, Rambold G, Elix JA (1995) A conspectus of the genus Phacopsis (Lecanorales). Bryologist 98:71–83. https://doi.org/10.2307/3243643
U'Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot 99:898–914. https://doi.org/10.3732/ajb.1100459
Van Den Broeck D, Ertz D (2016) Cryptophaea, a new genus of byssoid Arthoniaceae (lichenized Ascomycota) and its phylogenetic position. Phytotaxa 261:168–176. 10.11646/phytotaxa.261.2.6
Vilgalys R, Hester M (1990) Rapid gene identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
Vilgalys R, Sun BL (1994) Ancient and recent patterns of geographic speciation in the oyster mushroom Pleurotus revealed by phylogenetic analysis of ribosomal DNA sequences. PNAS 91:4599–4603. https://doi.org/10.1073/pnas.91.10.4599
Vainio EA (1903) Lichens. Expédition antarctique Belge. Résultats du voyage du S.Y. Belgica en 1897–1898–1899. Impr. JE Buschmann, pp 1–46.
Voglmayr H, Jaklitsch WM (2019) Stilbocrea walteri sp. nov., an unusual species of Bionectriaceae. Mycol Prog 18:91–105. https://doi.org/10.1007/s11557-018-1427-0
White TJ, Bruns T, Lee SB et al (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ et al (eds) PCR protocols: a guide to methods and application. Academic Press, San Diego, pp 315–322
Zoller S, Scheidegger C, Sperisen C (1999) PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming ascomycetes. Lichenologist 31:511–516. https://doi.org/10.1006/lich.1999.0220
Zhurbenko MP (2010) Lichenicolous fungi and lichens growing on Stereocaulon from the Holarctic, with a key to the known species. Opusc Philolichenum 8:9–39
Zhurbenko MP, Brackel WV (2013) Checklist of lichenicolous fungi and lichenicolous lichens of Svalbard, including new species, new records and revisions. Herzogia 26:323–359. https://doi.org/10.13158/heia.26.2.2013.323
Zhurbenko MP, Kobzeva AA (2014). Lichenicolous fungi from Northwest Caucasus, Russia. Herzogia 27:377–396. https://doi.org/10.13158/heia.27.2.2014.377
Zhurbenko MP, Ohmura Y (2019) New and interesting records of lichenicolous fungi from the TNS Herbarium: Part I. Opusc Philolichenum 18:74–89
Acknowledgements
We would like to acknowledge the excellent logistic support of the staff of Spanish Antarctic Station Juan Carlos I during our stay on Livingston Island. Fieldwork as well as some of the lab experiments were supported by the grants CTM2015–64728–C2–1–R and PID2019–105469RB–C21 (MINECO/FEDER, UE). The study was supported by Kew Future Leader Fellowship program. R. P-B. was supported by CAM Atracción de Talento program (2020-T1/AMB-19852). We are grateful to the lichenologists C. Printzen, U. Schiefelbein, and U. Søchting, who sent us some interesting specimens treated in this paper. We thank the referees for their detailed review and comments that helped us to improve the manuscript.
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This study was funded by the grants CTM2015–64728–C2–1–R, PID2019–105469RB–C21 (MINECO/FEDER, UE) and Kew Future Leader Fellowship program.
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JE collected specimens and conducted the morphological study. RPB conducted the molecular analyses. JE, RPB, and LS wrote the manuscript. All the authors read and approved the manuscript.
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Etayo, J., Sancho, L.G. & Pino-Bodas, R. Taxonomic and phylogenetic approach to some Antarctic lichenicolous fungi. Mycol Progress 22, 9 (2023). https://doi.org/10.1007/s11557-022-01860-7
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DOI: https://doi.org/10.1007/s11557-022-01860-7