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Symbiont composition of the basidiolichen Lichenomphalia meridionalis varies with altitude in the Iberian Peninsula

Published online by Cambridge University Press:  04 March 2020

Francisco Gasulla ,
José M. Barrasa ,
Leonardo M. Casano  and
Eva M. del Campo Open the ORCID record for Eva M. del Campo [Opens in a new window]
Francisco Gasulla
Affiliation:
Department of Life Sciences, University of Alcalá, 28805, Alcalá de Henares (Madrid), Spain
José M. Barrasa
Affiliation:
Department of Life Sciences, University of Alcalá, 28805, Alcalá de Henares (Madrid), Spain
Leonardo M. Casano
Affiliation:
Department of Life Sciences, University of Alcalá, 28805, Alcalá de Henares (Madrid), Spain
Eva M. del Campo*
Affiliation:
Department of Life Sciences, University of Alcalá, 28805, Alcalá de Henares (Madrid), Spain
*
Author for correspondence: Eva María del Campo. E-mail: eva.campo@uah.es
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Abstract

Basidiolichens are generally poorly researched because of the very small number of species and their restriction to special niches. Lichenomphalia basidiolichens grow in considerable quantities in arctic and alpine habitats but they are inadequately studied in these habitats in Mediterranean areas. Based on morphological and phylogenetic analyses, we identified the different symbionts of L. meridionalis, collected in localities in Spain at altitudes ranging from 533 to 2200 m above sea level. The present study provides the first molecular data available for L. meridionalis. We found that a microindel of six bp within the nrITS2 could help to discriminate L. meridionalis from other species of the genus. Molecular analyses revealed the existence of two different green algal strains, both belonging to Coccomyxa subellipsoidea, a species shared with other Lichenomphalia lichens. Notably, the two chlorobiont strains associated with L. meridionalis were differentially distributed according to altitude, and samples having one of the two strains consistently also included cyanobacteria.

Keywords

arctic-alpineCoccomyxacyanobacterialichenMediterraneansymbiosis
Type
Standard Papers
Information
The Lichenologist , Volume 52 , Issue 1 , January 2020 , pp. 17 - 26
Copyright
Copyright © British Lichen Society 2020

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References

Asplund, J and Wardle, DA (2015) Changes in functional traits of the terricolous lichen Peltigera aphthosa across a retrogressive boreal forest chronosequence. Lichenologist 47, 187–195.CrossRefGoogle Scholar
Barrasa, JM and Esteve-Raventós, F (2000) A redescription of Omphalina meridionalis, based on material collected in Spain. Mycotaxon 75, 273–280.Google Scholar
Barrasa, JM and Rico, VJ (2001) Lichenized species of Omphalina (Tricholomataceae) in the Iberian Peninsula. Lichenologist 33, 371–386.CrossRefGoogle Scholar
Barrasa, JM, Esteve-Raventós, F and Rico, VJ (2009) Lichenomphalia meridionalis comb. nov., a common and frequently misidentified species in south-western Europe. Lichenologist 41, 203–207.CrossRefGoogle Scholar
Blaha, J, Baloch, E and Grube, M (2006) High photobiont diversity associated with the euryoecious lichen-forming ascomycete Lecanora rupicola (Lecanoraceae, Ascomycota). Biological Journal of the Linnean Society 88, 283–293.CrossRefGoogle Scholar
Bold, HC and Parker, BC (1962) Some supplementary attributes in the classification of Chlorococcum species. Archives of Microbiology 42, 267–288.Google ScholarPubMed
Büdel, B and Scheidegger, C (2008) Thallus morphology and anatomy. In NashTH, III TH, III (ed.), Lichen Biology. Cambridge: Cambridge University Press, pp. 40–68.CrossRefGoogle Scholar
Casano, LM, del Campo, EM, García-Breijo, FJ, Reig-Arminana, J, Gasulla, F, Del Hoyo, A, Guéra, A and Barreno, E (2011) Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition? Environmental Microbiology 13, 806–818.CrossRefGoogle ScholarPubMed
Chapman, MJ and Margulis, L (1998) Morphogenesis by symbiogenesis. International Microbiology 1, 319–326.Google ScholarPubMed
Clement, M, Posada, D and Crandall, KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.CrossRefGoogle ScholarPubMed
Contu, M and La, Rocca S (1999) Fungi della zona mediterranea insulare italiana. Fungi non Delineati 9, 1–48.Google Scholar
Dal Forno, M, Lawrey, JD, Sikaroodi, M, Bhattarai, S, Gillevet, PM, Sulzbacher, M and Lücking, R (2013) Starting from scratch: evolution of the lichen thallus in the basidiolichen Dictyonema (Agaricales, Hygrophoraceae). Fungal Biology 117, 584–598.CrossRefGoogle Scholar
Dal Forno, M, Lücking, R, Bungartz, F, Yánez-Ayabaca, A, Marcelli, MP, Spielmann, AA, Coca, LF, Chaves, JL, Aptroot, A, Sipman, HJ, et al. (2016) From one to six: unrecognized species diversity in the genus Acantholichen (lichenized Basidiomycota: Hygrophoraceae). Mycologia 108, 38–55.CrossRefGoogle Scholar
Dal Grande, F, Rolshausen, G, Divakar, PK, Crespo, A, Otte, J, Schleuning, M and Schmitt, I (2018) Environment and host identity structure communities of green algal symbionts in lichens. New Phytologist 217, 277–289.CrossRefGoogle ScholarPubMed
Darienko, T, Gustavs, L, Eggert, A, Wolf, W and Pröschold, T (2015) Evaluating the species boundaries of green microalgae (Coccomyxa, Trebouxiophyceae, Chlorophyta) using integrative taxonomy and DNA barcoding with further implications for the species identification in environmental samples. PLoS ONE 10, e0127838.CrossRefGoogle ScholarPubMed
Ertz, D, Lawrey, JD, Sikaroodi, M, Gillevet, PM, Fischer, E, Killmann, D and Sérusiaux, E (2008) A new lineage of lichenized basidiomycetes inferred from a two-gene phylogeny: the Lepidostromataceae with three species from the tropics. American Journal of Botany 95, 1548–1556.CrossRefGoogle ScholarPubMed
Felsenstein, J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle ScholarPubMed
Gasulla, F, Guéra, A and Barreno, E (2010) A rapid and effective method for isolating lichen phycobionts into axenic culture. Symbiosis 51, 175–179.CrossRefGoogle Scholar
Geml, J, Kauff, F, Brochmann, C, Lutzoni, F, Laursen, GA, Redhead, SA and Taylor, DL (2012) Frequent circumarctic and rare transequatorial dispersals in the lichenised agaric genus Lichenomphalia (Hygrophoraceae, Basidiomycota). Fungal Biology 116, 388–400.CrossRefGoogle Scholar
Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.CrossRefGoogle ScholarPubMed
Hodkinson, BP, Moncada, B and Lücking, R (2014) Lepidostromatales, a new order of lichenized fungi (Basidiomycota, Agaricomycetes), with two new genera, Ertzia and Sulzbacheromyces, and one new species, Lepidostroma winklerianum. Fungal Diversity 64, 165–179.CrossRefGoogle Scholar
Honegger, R (1993) Developmental biology of lichens. New Phytologist 125, 659–677.CrossRefGoogle Scholar
Honegger, R (2012) The symbiotic phenotype of lichen-forming ascomycetes and their endo- and epibionts. In Hock, B (ed.), Fungal Associations. Berlin, Heidelberg: Springer, pp. 287–339.CrossRefGoogle Scholar
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.CrossRefGoogle ScholarPubMed
Kranner, I and Lutzoni, F (1999) Evolutionary consequences of transition to a lichen symbiotic state and physiological adaptation to oxidative damage associated with poikilohydry. In Lerner, HR (ed.), Plant Response to Environmental Stresses: from Phytohormones to Genome Reorganization. New York: Marcel Dekker, pp. 591–628.Google Scholar
Kroken, S and 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.CrossRefGoogle Scholar
Lawrey, JD, Lücking, R, Sipman, HJ, Chaves, JL, Redhead, SA, Bungartz, F, Sikaroodi, M and Gillevet, PM (2009) High concentration of basidiolichens in a single family of agaricoid mushrooms (Basidiomycota: Agaricales: Hygrophoraceae). Mycological Research 113, 1154–1171.CrossRefGoogle Scholar
Lefort, V, Longueville, JE and Gascuel, O (2017) SMS: Smart Model Selection in PhyML. Molecular Biology and Evolution 34, 2422–2424.CrossRefGoogle ScholarPubMed
Lodge, DJ, Padamsee, M, Matheny, PB, Aime, MC, Cantrell, SA, Boertmann, D, Kovalenko, A, Vizzini, A, Dentinger, BT and Kirk, PM (2014) Molecular phylogeny, morphology, pigment chemistry and ecology in Hygrophoraceae (Agaricales). Fungal Diversity 64, 1–99.CrossRefGoogle Scholar
Lücking, R, Dal-Forno, M, Sikaroodi, M, Gillevet, PM, Bungartz, F, Moncada, B, Yánez-Ayabaca, A, Chaves, JL, Coca, LF and Lawrey, JD (2014) A single macrolichen constitutes hundreds of unrecognized species. Proceedings of the National Academy of Sciences of the United States of America 111, 11091–11096.CrossRefGoogle ScholarPubMed
Lücking, R, Forno, MD, Moncada, B, Coca, LF, Vargas-Mendoza, L, Aptroot, A, Arias, LJ, Besal, B, Bungartz, F, Cabrera-Amaya, D, et al. (2017 a) Turbo-taxonomy to assemble a megadiverse lichen genus: seventy new species of Cora (Basidiomycota: Agaricales: Hygrophoraceae), honouring David Leslie Hawksworth's seventieth birthday. Fungal Diversity 84, 139–207.CrossRefGoogle Scholar
Lücking, R, Thorn, RG, Saar, I, Piercey-Normore, MD, Moncada, B, Doering, J, Mann, H, Lebeuf, R, Voitk, M and Voitk, A (2017 b) A hidden basidiolichen rediscovered: Omphalina oreades is a separate species in the genus Lichenomphalia (Basidiomycota: Agaricales: Hygrophoraceae). Lichenologist 49, 467–481.CrossRefGoogle Scholar
Malavasi, V, Skaloud, P, Rindi, F, Tempesta, S, Paoletti, M and Pasqualetti, M (2016) DNA-based taxonomy in ecologically versatile microalgae: a re-evaluation of the species concept within the coccoid green algal genus Coccomyxa (Trebouxiophyceae, Chlorophyta). PLoS ONE 11, e0151137.CrossRefGoogle Scholar
Nelsen, MP, Lücking, R, Umaña, L, Trest, MT, Will-Wolf, S, Chaves, JL and Gargas, A (2007) Multiclavula ichthyiformis (Fungi: Basidiomycota: Cantharellales: Clavulinaceae), a remarkable new basidiolichen from Costa Rica. American Journal of Botany 94, 1289–1296.CrossRefGoogle Scholar
Nimis, PL (1993) The Lichens of Italy: an Annotated Catalogue. Torino: Museo Regionale di Scienze Naturali di Torino.Google Scholar
Oberwinkler, F (2012) Basidiolichens. In Hock, B (ed.), Fungal Associations. Berlin, Heidelberg: Springer pp. 341–362.CrossRefGoogle Scholar
Penn, O, Privman, E, Landan, G, Graur, D and Pupko, T (2010 a) An alignment confidence score capturing robustness to guide tree uncertainty. Molecular Biology and Evolution 27, 1759–1767.CrossRefGoogle ScholarPubMed
Penn, O, Privman, E, Ashkenazy, H, Landan, G, Graur, D and Pupko, T (2010 b) GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Research 38, W23-8.CrossRefGoogle ScholarPubMed
Rambaut, A (2008) FigTree Version 1.3.1. [WWW resource] URL http://tree.bio.ed.ac.uk/software/figtree/.Google Scholar
Redhead, SA and Kuyper, TW (1987) Lichenized agarics: taxonomic and nomenclatural riddles. In Laursen, GA, Ammirati, JF and Redhead, SA (eds), Arctic and Alpine Mycology II. Boston, Massachusetts: Springer, pp. 319–348.CrossRefGoogle Scholar
Redhead, S, Moncalvo, J, Vilgalys, R and Lutzoni, F (2002) Phylogeny of agarics: partial systematics solutions for bryophilous omphalinoid agarics outside of the Agaricales (euagarics). Mycotaxon 82, 151–168.Google Scholar
Řeháková, K, Chlumská, Z and Doležal, J (2011) Soil cyanobacterial and microalgal diversity in dry mountains of Ladakh, NW Himalaya, as related to site, altitude, and vegetation. Microbial Ecology 62, 337–346.CrossRefGoogle ScholarPubMed
Reynolds, MM and Williams, CG (2004) Extracting DNA from submerged pine wood. Genome 47, 994–997.CrossRefGoogle ScholarPubMed
Sandoval-Leiva, P, Niveiro, N, Urbina-Casanova, R and Scherson, R (2017) Lichenomphalia altoandina, a new species of Hygrophoraceae from the Chilean Altiplano. Mycologia 109, 92–99.CrossRefGoogle ScholarPubMed
Suppan, U, Prügger, J and Mayrhofer, H (2000) Catalogue of the Lichenized and Lichenicolous Fungi of Slovenia. Stuttgart: Schweizerbart Science Publishers.Google Scholar
Tavaré, S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. In Miura, RM (ed.), Some Mathematical Questions in Biology - DNA Sequence Analysis. Providence, Rhode Island: American Mathematical Society, pp. 57–86.Google Scholar
Zoller, S and Lutzoni, F (2003) Slow algae, fast fungi: exceptionally high nucleotide substitution rate differences between lichenized fungi Omphalina and their symbiotic green algae Coccomyxa. Molecular Phylogenetics and Evolution 29, 629–640.CrossRefGoogle ScholarPubMed
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