Abstract
Lichenized fungi initiate their symbiotic structures from microscopic stages after recognition of compatible algae. The partnerships ultimately emerge as complex macroscopic phenotypes which are unrivaled in the fungal kingdom by their resilience and durability. This chapter presents an overview of lichen symbioses and covers the morphology and systematics of the fungal phenotypes, as well as their associations with diverse photobionts. This is followed by a coarse overview of ecophysiology and the secondary chemistry. A special focus is given to the diversity of and the interactions with additional microorganisms. Finally, a few comments on the effects of pollution and environmental change point to the usefulness of lichens as bioindicators.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abdel-Hameed M, Bertrand RL, Piercey-Normore MD, Sorensen JL (2016) Putative identification of the usnic acid biosynthetic gene cluster by de novo whole-genome sequencing of a lichen-forming fungus. Fungal Biol 120:306–316
Ahmadjian V (1993) The lichen symbiosis. Wiley, New York
Ahmadjian V, Jacobs JB (1981) Relationship between fungus and alga in the lichen Cladonia cristatella Tuck. Nature 289:169–172
Ahmadjian V, Russel LA, Hildreth KC (1980) Artificial reestablishment of lichens. I. Morphological interactions between the phycobionts of different lichens and the mycobionts Cladonia cristatella and Lecanora chrysoleuca. Mycologia 72:73–89
Anderson OR (2014) Microbial communities associated with tree bark foliose lichens: a perspective on their microecology. J Eukar Microbiol 61:364–370
Armaleo D, Chiou L (2021) Modeling in yeast how rDNA introns slow growth and increase desiccation tolerance in lichens. G3 11:jkab279
Armaleo D, Sun X, Culberson C (2011) Insights from the first putative biosynthetic gene cluster for a lichen depside and depsidone. Mycologia 103:741–754
Armaleo D, Müller O, Lutzoni F, Andrésson ÓS, Blanc G, Bode HB, Collart FR, Dal Grande F, Dietrich F, Grigoriev IV, Joneson S, Kuo A, Larsen PE, Logsdon JM Jr, Lopez D, Martin F, May SP, McDonald TR, Merchant SS, Miao V, Morin E, Oono R, Pellegrini M, Rubinstein N, Sanchez-Puerta MV, Savelkoul E, Schmitt I, Slot JC, Soanes D, Szövényi P, Talbot NJ, Veneault-Fourrey C, Xavier BB (2019) The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata. BMC Genomics 20:1–33
Arup U, Søchting U, Frödén P (2013) A new taxonomy of the family Teloschistaceae. Nordic J Bot 31:16–83
Aschenbrenner IA, Cardinale M, Berg G, Grube M (2014) Microbial cargo: do bacteria on symbiotic propagules reinforce the microbiome of lichens? Environ Microbiol 16:3743–3752
Asplund J, Wardle DA (2017) How lichens impact on terrestrial community and ecosystem properties. Biol Rev 92:1720–1738
Bačkor M, Loppi S (2009) Interactions of lichens with heavy metals. Biol Plant 53:214–222
Bates ST, Cropsey GW, Caporaso JG, Knight R, Fierer N (2011) Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 77:1309–1314
Beckett RP, Minibayeva FV, Laufer Z (2005) Extracellular reactive oxygen species production by lichens. Lichenologist 37:397–407
Berkeley MJ (1844) Notices of British fungi. Ann Mag Nat Hist 13:340–360
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
Blum OB, Kashevarov GP (1986) The DNA homologies as a proof of the legitimacy of the establishment of the lichen genus Lasallia Merat (Umbilicariaceae). Doklady Akademii Nauk Ukrainskoi SSR Seriya B 12:61–64
Borgato L, Ertz D, Van Rossum F, Verbeken A (2022) The diversity of lichenized trentepohlioid algal (Ulvophyceae) communities is driven by fungal taxonomy and ecological factors. J Phycol 58(4):582–602
Brunauer G, Muggia L, Stocker-Wörgötter E, Grube M (2009) A transcribed polyketide synthase gene from Xanthoria elegans. Mycol Res 113:82–92
Candotto Carniel F, Fernandez-Marín B, Arc E, Craighero T, Laza JM, Incerti G, Tretiach M, Kranner I (2021) How dry is dry? Molecular mobility in relation to thallus water content in a lichen. J Exp Bot 72:1576–1588
Cardinale M, Puglia AM, Grube M (2006) Molecular analysis of lichen-associated bacterial communities. FEMS Microbiol Ecol 57:484–495
Cardinale M, Vieira de Castro J Jr, Müller H, Berg G, Grube M (2008) In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol Ecol 66:63–71
Cardinale M, Steinová J, Rabensteiner J, Berg G, Grube M (2012) Age, sun and substrate: triggers of bacterial communities in lichens. Environ Microbiol Rep 4:23–28
Casano LM, del Campo EM, García-Breijo FJ, Reig-Armiñana J, Gasulla F, Del Hoyo A, Guéro 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
Cengia Sambo M (1926) Ancora della polisimbiosi nei licheni ad alghe cianoficee. 1. Batteri simbionti. Atti Soc Ital Sci Nat Mus Civ Storia Nat Milano 64:191–195
Cernava T, Erlacher A, Aschenbrenner IA, Krug L, Lassek C, Riedel K, Grube M, Berg G (2017) Deciphering functional diversification within the lichen microbiota by meta-omics. Microbiome 5:1–13
Cernava T, Aschenbrenner IA, Soh J, Sensen CW, Grube M, Berg G (2019) Plasticity of a holobiont: desiccation induces fasting-like metabolism within the lichen microbiota. ISME J 13:547–556
Colesie C, Williams L, Büdel B (2017) Water relations in the soil crust lichen Psora decipiens are optimized via anatomical variability. Lichenologist 49:483–492
Conti ME (2008) Lichens as bioindicators of air pollution. WIT Transact State-of-the-art Sci Engin 30:111–162
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 217:277–289
Dal-Forno M, Lawrey JD, Sikaroodi M, Bhattarai S, Gillevet PM, Sulzbacher M, Lücking R (2013) Starting from scratch: evolution of the lichen thallus in the basidiolichen Dictyonema (Agaricales: Hygrophoraceae). Fungal Biol 117:584–598
Darnajoux R, Zhang X, McRose DL, Miadlikowska J, Lutzoni F, Kraepiel AM, Bellenger JP (2017) Biological nitrogen fixation by alternative nitrogenases in boreal cyanolichens: importance of molybdenum availability and implications for current biological nitrogen fixation estimates. New Phytol 213:680–689
De Los Ríos A, Ascaso C, Grube M (2002a) Infection mechanisms of lichenicolous fungi studied by various microscopic techniques. Biblioth Lichenol 82:153–161
De Los Ríos A, Ascaso C, Grube M (2002b) An ultrastructural, anatomical and molecular study of the lichenicolous lichen Rimularia insularis. Mycol Res 106:946–953
Demmig-Adams B, Maguas C, Adams WW, Meyer A, Kilian E, Lange OL (1990a) Effect of high light on the efficiency of photochemical energy conversion in a variety of lichen species with green and blue-green phycobionts. Planta 180:400–409
Demmig-Adams B, Adams WW, Green TGA, Czygan FC, Lange OL (1990b) Differences in the susceptibility to light stress in two lichens forming a phycosymbiodeme, one partner possessing and one lacking the xanthophyll cycle. Oecologia 84:451–456
Díaz-Escandón D, Tagirdzhanova G, Vanderpool D, Allen CCG, Aptroot A, Češka O, Hawksworth DL, Huereca A, Knudsen K, Kocourková J, Lücking R, Resl P, Spribille T (2022) Genome-level analyses resolve an ancient lineage of symbiotic ascomycetes. Curr Biol 32:5209–5218
Diederich P, Lawrey JD, Ertz D (2018) The 2018 classification and checklist of lichenicolous fungi, with 2000 non-lichenized, obligately lichenicolous taxa. Bryologist 121:340–425
Dietz S, Büdel B, Lange OL, Bilger W (2000) Transmittance of light through the cortex of lichens from contrasting habitats. Bibl Lichenol 75:171–182
Du ZY, Zienkiewicz K, Vande Pol N, Ostrom NE, Benning C, Bonito GM (2019) Algal-fungal symbiosis leads to photosynthetic mycelium. elife 8:e47815
Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462
Ellis CJ, Crittenden PD, Scrimgeour CM, Ashcroft CJ (2005) Translocation of 15N indicates nitrogen recycling in the mat-forming lichen Cladonia portentosa. New Phytol 168:423–434
Ertz D, Guzow-Krzemińska B, Thor G, Łubek A, Kukwa M (2018) Photobiont switching causes changes in the reproduction strategy and phenotypic dimorphism in the Arthoniomycetes. Sci Rep 8:1–14
Esseen PA, Ekström M, Grafström JBG, Palmquist K, Westerlund B, Stahl G (2022) Multiple drivers of large-scale decline in boreal forest canopies. Glob Change Biol 28:3293–3309
Eymann C, Lassek C, Wegner U, Bernhardt J, Fritsch OA, Fuch S, Otto A, Albrecht D, Schiefelbein U, Cernava T, Aschenbrenner I, Berg G, Grube M, Riedel K (2017) Symbiotic interplay of fungi, algae, and bacteria within the lung lichen Lobaria pulmonaria L. Hoffm. as assessed by state-of-the-art metaproteomics. J Prot Res 16:2160–2173
Farrant JM, Hilhorst HW (2021) What is dry? Exploring metabolism and molecular mobility at extremely low water contents. J Exp Bot 72:1507–1510
Farrar JF (1976) The lichen as an ecosystem: observation and experiment. In: Brown DH, Hawksworth DL, Bailey RH (eds) Lichenology: progress and problems. Academic, London, pp 385–406
Fernández-Mendoz F, Fleischhacker A, Kopun T, Grube M, Muggia L (2017) ITS 1 metabarcoding highlights low specificity of lichen mycobiomes at a local scale. Mol Ecol 26:4811–4830
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
Fernandez-Mendoza F, Strasser E, Frolov I, Vondrak J, Muggia L, Mayrhofer H, Gaya E, Grube M (2023) Introgressive descent and hypersexuality drive the evolution of sexual parasitism and morphological reduction in a fungal species complex. bioRxiv, 2023-01
Ferraro LI (2004) Morphological diversity in the hyphophores of Gomphillaceae (Ostropales, lichenized Ascomycetes). Fungal Div 15:153–169
Frank AB (1876) Über die biologischen Verhältnisse des Thallus einiger Krustenflechten. Cohn, Beitr Biol Pflanzen 2:123–200
Friedl T (1989) Systematik und Biologie von Trebouxia (Microthamniales, Chlorophyta) als Phycobiont der Parmeliaceae (lichenisierte Ascomyceten). 218p. Doctoral thesis, Universität Bayreuth
Gadea A, Fanuel M, Lamer A-CL, Boustie J, Rogniaux H, Charrier M, Devehat FL-L (2020) Mass spectrometry imaging of specialized metabolites for predicting lichen fitness and snail foraging. Plan Theory 9:70
García-Plazaola JI, Esteban R, Fernández-Marín B, Kranner I, Porcar-Castell A (2012) Thermal energy dissipation and xanthophyll cycles beyond the Arabidopsis model. Photosynth Res 113:89–103
Garg N, Zeng Y, Edlund A, Melnik AV, Sanchez LM, Mohimani H, Gurevich A, Miao V, Schiffler S, Lim YW, Luzzatto-Knaan T, Cai S, Rohwer F, Pevzner PA, Cichewicz RH, Alexandrov T, Dorrestein PC (2016) Spatial molecular architecture of the microbial community of a Peltigera lichen. mSystems 1:e00139–e00116
Gargas A, Taylor JW (1992) Polymerase chain reaction (PCR) primers for amplifying and sequencing nuclear 18s rDNA from lichenized fungi. Mycologia 84:589–592
Gargas A, DePriest PT, Grube M, Tehler A (1995) Multiple origins of lichen symbioses in fungi suggested by SSU rDNA phylogeny. Science 268:1492–1495
Garrido-Benavent I, Pérez-Ortega S, de los Ríos A, Fernández-Mendoza F (2020) Amphitropical variation of the algal partners of Pseudephebe (Parmeliaceae, lichenized fungi). Symbiosis 82:35–48
Gasulla F, Barrasa JM, Casano LM, del Campo EM (2020) Symbiont composition of the basidiolichen Lichenomphalia meridionalis varies with altitude in the Iberian Peninsula. Lichenologist 52:17–26
González I, Ayuso-Sacido A, Anderson A, Genilloud O (2005) Actinomycetes isolated from lichens: evaluation of their diversity and detection of biosynthetic gene sequences. FEMS Microbiol Ecol 54:401–415
González-Hourcade M, Braga MR, Del Campo EM, Ascaso C, Patiño C, Casano LM (2020) Ultrastructural and biochemical analyses reveal cell wall remodelling in lichen-forming microalgae submitted to cyclic desiccation–rehydration. Ann Bot 125:459–469
Gostinčar C, Muggia L, Grube M (2012) Polyextremotolerant black fungi: oligotrophism, adaptive potential, and a link to lichen symbioses. Front Microbiol 3:390
Green TGA, Schroeter B, Kappen L, Seppelt RD, Maseyk K (1998) An assessment of the relationship between chlorophyll a fluorescence and CO2 gas exchange from field measurements on a moss and lichen. Planta 206:611–618
Green TGA, Nash TH, Lange OL (2008) Physiological ecology of carbon dioxide exchange. In: Nash TH (ed) Lichen biology. Cambridge University Press, New York, pp 152–181
Grube M, Arup U (2001) Molecular and morphological evolution in the Physciaceae (Lecanorales, lichenized Ascomycotina), with special emphasis on the genus Rinodina. Lichenologist 33:63–72
Grube M, Hawksworth DL (2007) Trouble with lichen: the re-evaluation and re-interpretation of thallus form and fruit body types in the molecular era. Mycol Res 111:1116–1132
Grube M, Kantvilas G (2006) Siphula represents a remarkable case of morphological convergence in sterile lichens. Lichenologist 38:241–249
Grube M, Cardinale M, de Castro JV, Müller H, Berg G (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J 3:1105–1115
Grube M, Cernava T, Soh J, Fuchs S, Aschenbrenner I, Lassek C, Wegner U, Becher D, Riedel K, Sensen CW, Berg G (2015) Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics. ISME J 9:412–424
Grube M, Muggia L, Baloch E, Hametner C, Stocker-Wörgötter E (2017) Symbioses of lichen-forming fungi with Trentepohlialean algae. In: Grube M, Seckbach J, Muggia L (eds) Algal and cyanobacteria symbioses. World Scientific, Hackensack, NJ, pp 85–110
Gustavs L, Schiefelbein U, Darienko PT (2017) Symbioses of the green algal genera Coccomyxa and Elliptochloris (Trebouxiophyceae, Chlorophyta). In: Grube M, Seckbach J, Muggia L (eds) Algal and cyanobacteria symbioses. World Scientific, Hackensack, NJ, pp 169–208
Hafellner J (2018) Focus on lichenicolous fungi: Diversity and taxonomy under the principle “one fungus – one name”. In Blanz P (ed) Biodiversity and ecology of fungi, lichens, and mosses, Austrian Academy of Sciences Biosystematics and Ecology Series. 34. Austrian Academy of Sciences, Vienna, pp 227–244
Hametner C, Stocker-Wörgötter E, Grube M (2014a) New insights into diversity and selectivity of trentepohlialean lichen photobionts from the extratropics. Symbiosis 63:31–40
Hametner C, Stocker-Wörgötter E, Rindi F, Grube M (2014b) Phylogenetic position and morphology of lichenized Trentepohliales (Ulvophyceae, Chlorophyta) from selected species of Graphidaceae. Phycol Res 62:170–186
Hawksworth DL, Grube M (2020) Lichens redefined as complex ecosystems. New Phytol 227:1281
Henkel PA, Yuzhakova LA (1936) Azotfiksiruyuschie bakterii v lishaynikah. Izv Biol Inst Permsk Gos Univ 10:9–10
Henskens FL, Green TA, Wilkins A (2012) Cyanolichens can have both cyanobacteria and green algae in a common layer as major contributors to photosynthesis. Ann Bot 110:555–563
Hodkinson BP, Gottel NR, Schadt CW, Lutzoni F (2012) Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ Microbiol 14:147–161
Hodkinson BP, Allen JL, Forrest LL, Goffinet B, Sérusiaux E, Andrésson ÓS, Miao V, Bellenger JP, Lutzoni F (2014) Lichen-symbiotic cyanobacteria associated with Peltigera have an alternative vanadium-dependent nitrogen fixation system. Eur J Phycol 49:11–19
Honegger R (1991) Functional aspects of the lichen symbiosis. Annu Rev Plant Biol 42:553–578
Honegger R (2012) The symbiotic phenotype of lichen-forming ascomycetes and their endo- and epibionts. In: Hock B (ed) The Mycota IX. Springer, Berlin, pp 287–339
Honegger R, Edwards D, Axe L (2013) The earliest records of internally stratified cyanobacterial and algal lichens from the Lower Devonian of the Welsh Borderland. New Phytol 197:264–275
Hyvärinen M, Crittenden PD (2000) 33P translocation in the thallus of the mat-forming lichen Cladonia portentosa. New Phytol 145:281–288
Hyvärinen M, Härdling R, Tuomi J (2002) Cyanobacterial lichen symbiosis: the fungal partner as an optimal harvester. Oikos 98:498–504
Johansson O, Olofsson J, Giesler R, Palmqvist K (2011) Lichen responses to nitrogen and phosphorus additions can be explained by the different symbiont responses. New Phytol 191:795–805
Joneson S, Lutzoni F (2009) Compatibility and thigmotropism in the lichen symbiosis: a reappraisal. Symbiosis 47:109–115
Joneson S, Armaleo D, Lutzoni F (2011) Fungal and algal gene expression in early developmental stages of lichen-symbiosis. Mycologia 103:291–306
Kaasalainen U, Tuovinen V, Mwachala G, Pellikka P, Rikkinen J (2021) Complex interaction networks among cyanolichens of a tropical biodiversity hotspot. Front Microbiol 12:672333
Kauppi M, Verseghy-Patay K (1990) Determination of the distribution of lichen substances in the thallus by fluorescence microscopy. Ann Bot Fenn 27:189–202
Kershaw KA (1985) Physiological ecology of lichens. Cambridge University Press, Cambridge
Keuler R, Garretson A, Saunders T, Erickson RJ, St Andre N, Grewe F, Smith H, Lumbsch HT, Huang J-P, Leavitt SD (2020) Genome-scale data reveal the role of hybridization in lichen-forming fungi. Sci Rep 10:1–14
Kim W, Liu R, Woo S, Kang KB, Park H, Yu YH, Ha HH, Oh SY, Yang JH, Kim H, Yun SH, Hur JS (2021) Linking a gene cluster to atranorin, a major cortical substance of lichens, through genetic dereplication and heterologous expression. MBio 12:e01111–e01121
Kohlmeyer J, Hawksworth DL, Volkmann-Kohlmeyer B (2004) Observations on two marine and maritime “borderline” lichens: Mastodia tessellata and Collemopsidium pelvetiae. Mycol Prog 3:51–56
Kono M, Kon Y, Ohmura Y, Satta Y, Terai Y (2020) In vitro resynthesis of lichenization reveals the genetic background of symbiosis-specific fungal-algal interaction in Usnea hakonensis. BMC Genomics 21:1–16
Kosecka M, Jabłońska A, Flakus A, Rodriguez-Flakus P, Kukwa M, Guzow-Krzemińska B (2020) Trentepohlialean algae (Trentepohliales, Ulvophyceae) show preference to selected mycobiont lineages in lichen symbioses. J Phycol 56:979–993
Kranner I, Cram WJ, Zorn M, Wornik S, Yoshimura I, Stabentheiner E, Pfeifhofer H (2005) Antioxidants and photoprotection in a lichen as compared to its isolated symbiotic partners. PNAS 102:3141–3146
Kranner I, Beckett R, Hochman A, Nash TH III (2008) Desiccation-tolerance in lichens: a review. Bryologist 111:576–593
Kroken S, Taylor JW (2001) A gene genealogical approach to recognize phylogenetic species boundaries in the lichenized fungus Letharia. Mycologia 93:38–53
Lakatos M, Lange-Bertalot H, Büdel B (2004) Diatoms living inside the thallus of the green algal lichen Coenogonium linkii in neotropical lowland rain forests. J Phycol 40:70–73
Lambers H (1985) Respiration in intact plants and tissues: its regulation and dependence on environmental factors, metabolism and invaded organisms. In: Douce R, Day DA (eds) Higher Plant Respiration. Springer, Berlin, pp 418–465
Larson DW (1987) The absorption and release of water by lichens. Bibl Lichenol 25:351–360
Leiva D, Fernández-Mendoza F, Acevedo J, Carú M, Grube M, Orlando J (2021) The bacterial community of the foliose macro-lichen Peltigera frigida is more than a mere extension of the microbiota of the subjacent substrate. Microb Ecol 81:965–976
Liba CM, Ferrara FIDS, Manfio GP, Fantinatti-Garboggini F, Albuquerque RC, Pavan C, Ramos PL, Moreira-Filho CA, Barbosa HR (2006) Nitrogen-fixing chemo-organotrophic bacteria isolated from cyanobacteria-deprived lichens and their ability to solubilize phosphate and to release amino acids and phytohormones. J Appl Microbiol 101:1076–1086
Lücking L, Grube M (2002) Facultative parasitism and reproductive strategies in Chroodiscus (Ascomycota, Ostropales). Stapfia 80:267–292
Lücking R, Dal-Forno M, Sikaroodi M, Gillevet PM, Bungartz F, Moncada B, Yánez-Ayabaca A, Chaves JL, Coca LF, Lawrey JD (2014) A single macrolichen constitutes hundreds of unrecognized species. PNAS 111:11091–11096
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
Lutzoni F, Pagel M, Reeb V (2001) Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411:937–940
Mark K, Laanisto L, Bueno CG, Niinemets Ü, Keller C, Scheidegger C (2020) Contrasting co-occurrence patterns of photobiont and cystobasidiomycete yeast associated with common epiphytic lichen species. New Phytol 227:1362–1375
Matthews SW, Tucker SC, Chapman RL (1989) Ultrastructural features of mycobionts and trentepohliaceous phycobionts in selected subtropical crustose lichens. Bot Gaz 150:417–438
Meeßen J, Eppenstein S, Ott S (2013) Recognition mechanisms during the pre-contact state of lichens: II. Influence of algal exudates and ribitol on the response of the mycobiont of Fulgensia bracteata. Symbiosis 59:131–143
Merges D, Dal Grande F, Greve C, Otte J, Schmitt I (2021) Virus diversity in metagenomes of a lichen symbiosis (Umbilicaria phaea): complete viral genomes, putative hosts and elevational distributions. Environ Microbiol 23:6637–6650
Moya P, Molins A, Chiva S, Bastida J, Barreno E (2020) Symbiotic microalgal diversity within lichenicolous lichens and crustose hosts on Iberian Peninsula gypsum biocrusts. Sci Rep 10:1–14
Muggia L, Nelson P, Wheeler T, Yakovchenko LS, Tønsberg T, Spribille T (2011) Convergent evolution of a symbiotic duet: the case of the lichen genus Polychidium (Peltigerales, Ascomycota). Am J Bot 98:1647–1656
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
Muggia L, Leavitt S, Barreno E (2018) The hidden diversity of lichenised Trebouxiophyceae (Chlorophyta). Phycologia 57:503–524
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 Phylogen Evol 149:106821
Nascimbene J, Benesperi R, Giordani P, Grube M, Marini L, Vallese C, Mayrhofer H (2019) Could hair-lichens of high-elevation forests help detect the impact of global change in the Alps? Diversity 11:45
Nash T (2008) Nutrients, elemental accumulation, and mineral cycling. In: Nash T (ed) Lichen biology, 2nd edn. Cambridge University Press, Cambridge, pp 234–251
Nelsen MP, Plata ER, Andrew CJ, Lücking R, Lumbsch HT (2011) Phylogenetic diversity of trentepohlialean algae associated with lichen-forming fungi. J Phycol 47:282–290
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 18:3–13
Nelsen MP, Leavitt SD, Heller K, Muggia L, Lumbsch HT (2022) Contrasting patterns of climatic niche divergence in Trebouxia—a clade of lichen-forming algae. Front Microbiol 13:791546
Nguyen VK, Genta-Jouve G, Duong TH, Beniddir MA, Gallard JF, Ferron S, Boustie J, Mouray E, Grellier P, Chavasiri W, Le Pogam P (2020) Eumitrins C-E: structurally diverse xanthone dimers from the Vietnamese lichen Usnea baileyi. Fitoterapia 141:104449
Nylander W (1857) De fungillis binis lichenicolis observatio. Bot Not 1857:83–84
Oberwinkler F (2012) Basidiolichens. In: Hock B (ed) Fungal associations. Springer, Berlin, pp 341–362
Oliver MJ, Farrant JM, Hilhorst HWM, Mundree S, Williams B, Bewley JD (2020) Desiccation tolerance: avoiding cellular damage during drying and rehydration. Ann Rev Plant Biol 71:435–460
Peksa O, Gebouská T, Škvorová Z, Vančurová L, Škaloud P (2022) The guilds in green algal lichens—an insight into the life of terrestrial symbiotic communities. FEMS Microbiol Ecol 98(2):fiac008
Petrini O, Hake U, Dreyfuss MM (1990) An analysis of fungal communities isolated from fruticose lichens. Mycologia 82:444–451
Petrzik K, Vondrák J, Barták M, Peksa O, Kubešová O (2014) Lichens, a new source or yet unknown host of herbaceous plant viruses? Eur J Plant Pathol 138:549–559
Petrzik K, Vondrák J, Kvíderová J, Lukavský J (2015) Platinum anniversary: virus and lichen alga together more than 70 years. PLoS One 10:3
Petrzik K, Koloniuk I, Sarkisová T, Èíhal L (2016) Detection of herbaceous-plant pararetrovirus in lichen herbarium samples. Acta Virol 60:196–200
Petrzik K, Koloniuk I, Sehadová H, Sarkisova T (2019) Chrysoviruses inhabited symbiotic fungi of lichens. Viruses 11:12
Peveling E (1970) Die Darstellung der Oberflächenstrukturen von Flechten mit dem Raster-Elektronenmikroskop. Deutsche Bot Ges NF 4:89–101
Pichler G, Muggia L, Candotto Carniel F, Grube M, Kranner I (2023) How to build a lichen: from metabolite release to symbiotic interplay. New Phytol 238:1362–1378
Pizarro D, Divakar PK, Grewe F, Crespo A, Dal Grande F, Lumbsch HT (2020) Genome-wide analysis of biosynthetic gene cluster reveals correlated gene loss with absence of usnic acid in lichen-forming fungi. Genome Biol Evol 12:1858–1868
Poelt J, Mayrhofer H (1988) Über Cyanotrophie bei Flechten. Plant Syst Evol 158:265–281
Ponsero AJ, Hurwitz BL, Magain N, Miadlikowska J, Lutzoni F, U’Ren JM (2021) Cyanolichen microbiome contains novel viruses that encode genes to promote microbial metabolism. ISME Commun 1:1–4
Printzen C, Ekman S, Tønsberg T (2003) Phylogeography of Cavernularia hultenii: evidence of slow genetic drift in a widely disjunct lichen. Mol Ecol 12:1473–1486
Rai AN (2002) Cyanolichens: nitrogen metabolism. In: Rai AM, Bergman B, Rasmusson U (eds) Cyanobacteria in symbiosis. Springer, Dordrecht, pp 97–115
Reich PB, Walters MB, Ellsworth DS, Vose JM, Volin JV, Gresham C, Bowman WD (1998) Relationships of leaf dark respiration to leaf nitrogen, specific leaf area and leaf life-span: a test across biomes and functional groups. Oecologia 114:471–482
Resl P, Bujold AR, Tagirdzhanova G, Meidl P, Freire Rallo S, Kono M, Fernández-Brime S, Guðmundsson H, Andrésson ÓS, Muggia L, Mayrhofer H, McCutcheon JP, Wedin M, Werth S, Willis LM, Spribille T (2022) Large differences in carbohydrate degradation and transport potential among lichen fungal symbionts. Nat Commun 13:2634
Rikkinen J (2017) Cyanobacteria in terrestrial symbiotic systems. In: Hallenbeck PC (ed) Modern topics in the phototrophic prokaryotes. Springer, Cham, pp 243–294
Sanders WB (2014) Complete life cycle of the lichen fungus Calopadia puiggarii (Pilocarpaceae, Ascomycetes) documented in situ: Propagule dispersal, establishment of symbiosis, thallus development, and formation of sexual and asexual reproductive structures. Am J Bot 101:1836–1848
Sanders WB, Ascaso C (1995) Reiterative production and deformation of cell walls in expanding thallus nets of the lichen Ramalina menziesii (Lecanorales, Ascomycetes). Am J Bot 82:1358–1366
Sanders WB, Masumoto H (2021) Lichen algae: the photosynthetic partners in lichen symbioses. Lichenologist 53:347–393
Schaper GM, Ott S (2003) Photobiont selectivity and interspecific in interactions in lichen communities. Culture experiments with the mycobiont Fulgensia bracteata. Plant Biol 5:441–450
Scherrer S, Honegger R (2003) Inter- and intraspecific variation of homologous hydrophobin (H1) gene sequences among Xanthoria spp. (lichen-forming ascomycetes). New Phytol 158:375–389
Scherrer S, De Vries OMH, Dudler R, Wessels JGH, Honegger R (2000) Interfacial self-assembly of fungal hydrophobins of the lichen-forming ascomycetes Xanthoria parietina and X. ectaneoides. Fungal Genet Biol 30:81–93
Schmitt I, Lumbsch HT (2009) Ancient horizontal gene transfer from bacteria enhances biosynthetic capabilities of fungi. PLoS One 4:e4437
Schüßler A, Kluge M (2001) Geosiphon pyriforme, an endocytosymbiosis between fungus and cyanobacteria, and its meaning as a model system for arbuscular mycorrhizal research. In: Hock B (ed) The Mycota 9: fungal associations. Springer, Berlin, pp 151–161
Schwendener S (1869) Die Algentypen der Flechtengonidien. C. Schultze
Singh G, Calchera A, Schulz M, Drechsler M, Bode HB, Schmitt I, Dal Grande F (2021) Climate-specific biosynthetic gene clusters in populations of a lichen-forming fungus. Environ Microbiol 23:4260–4275
Singh G, Calchera A, Merges D, Valim H, Otte J, Schmitt I, Dal Grande F (2022) A candidate gene cluster for the bioactive natural product gyrophoric acid in lichen-forming fungi. Microbiol Spectr. https://doi.org/10.1128/spectrum.00109-22
Škvorová Z, Černajová I, Steinová J, Peksa O, Moya P, Škaloud P (2022) Promiscuity in lichens follows clear rules: partner switching in Cladonia is regulated by climatic factors and soil chemistry. Front Microbiol 12:781585
Spribille T, Tuovinen V, Resl P, Vanderpool D, Wolinski H, Aime MC, Schneider K, Stabentheiner E, Toome-Heller M, Thor G, Mayrhofer H, Johannesson H, McCutcheon J (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353:488–492
Spribille T, Tagirdzhanova G, Goyette S, Tuovinen V, Case R, Zandberg WF (2020) 3D biofilms: in search of the polysaccharides holding together lichen symbioses. FEMS Microbiol Lett 367:5
Steinová J, Holien H, Košuthová A, Škaloud P (2022) An exception to the rule? Could photobiont identity be a better predictor of lichen phenotype than mycobiont identity? J Fungi 8:275
Stocker-Wörgötter E (2001) Experimental lichenology and microbiology of lichens: culture experiments, secondary chemistry of cultured mycobionts, resynthesis, and thallus morphogenesis. Bryologist 104:576–581
Thaxter R (1892) On the Myxobacteriaceae, a new order of Schizomycetes. Bot Gaz 17:389–406
Trembley ML, Ringli C, Honegger R (2002) Hydrophobins DGH1, DGH2, and DGH3 in the lichen-forming basidiomycete Dictyonema glabratum. Fungal Genet Biol 35:247–259
Tripathi M, Joshi Y (2019) Endolichenic fungi: present and future trends. Springer, Singapore
Tuong TL, Do LT, Aree T, Wonganan P, Chavasiri W (2020) Tetrahydroxanthone–chromanone heterodimers from lichen Usnea aciculifera and their cytotoxic activity against human cancer cell lines. Fitoterapia 147:104732
Tuovinen V, Millanes AM, Freire-Rallo S, Rosling A, Wedin M (2021) Tremella macrobasidiata and Tremella variae have abundant and widespread yeast stages in Lecanora lichens. Environ Microbiol 23:2484–2498
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
Urayama SI, Doi N, Kondo F, Chiba Y, Takaki Y, Hirai M, Minegshi Y, Hagiwara D, Nunoura T (2020) Diverged and active partitiviruses in lichen. Front Microbiol 11:561344
Velmala S, Myllys L, Halonen P, Goward T, Ahti T (2009) Molecular data show that Bryoria fremontii and B. tortuosa (Parmeliaceae) are conspecific. Lichenologist 41:231–242
Vondrak J, Kubásek J (2013) Algal stacks and fungal stacks as adaptations to high light in lichens. Lichenologist 45:115–124
Walser JC (2004) Molecular evidence for limited dispersal of vegetative propagules in the epiphytic lichen Lobaria pulmonaria. Am J Bot 91:1273–1276
Wedin M, Döring H, Gilenstam G (2004) Saprotrophy and lichenization as options for the same fungal species on different substrata: environmental plasticity and fungal lifestyles in the Stictis–Conotrema complex. New Phytol 164:459–465
Wedin M, Maier S, Fernandez-Brime S, Cronholm B, Westberg M, Grube M (2016) Microbiome change by symbiotic invasion in lichens. Environ Microbiol 18:1428–1439
Wilkinson DM, Creevy AL, Kalu CL, Schwartzman DW (2015) Are heterotrophic and silica-rich eukaryotic microbes an important part of the lichen symbiosis? Mycology 6:4–7
Wirth V, Hauck M, Schultz M (2013) Die Flechten Deutschlands, vol Band 1. Ulmer, Stuttgart
Yamamoto Y, Kinoshita Y, Thor G, Hasumi M, Kinoshita K, Koyama K, Takahashi K, Yoshimura I (2002) Isofuranonaphthoquinone derivatives from cultures of the lichen Arthonia cinnabarina (DC.) Wallr. Phytochemistry 60:741–745
Yuan X, Xiao S, Taylor TN (2005) Lichen-like symbiosis 600 million years ago. Science 308:1017–1020
Zopf W (1897) Ueber Nebensymbiose (Parasymbiose). Ber Deutsch Bot Ges 15:90–92
Acknowledgments
The author thank Fernando Fernandez Mendoza (Graz) for discussions and Ilse Kranner (Innsbruck) for comments on the text.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2024 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Grube, M. (2024). Lichens. In: Hsueh, YP., Blackwell, M. (eds) Fungal Associations. The Mycota, vol 9. Springer, Cham. https://doi.org/10.1007/978-3-031-41648-4_6
Download citation
DOI: https://doi.org/10.1007/978-3-031-41648-4_6
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-41647-7
Online ISBN: 978-3-031-41648-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)