Crustose Verrucariaceae lichens form a distinctive black belt on seashores all over the world. This lifestyle is apparently enabled by a specific set of photobionts. However, their diversity is understudied. We sampled these lichens from the northern Patagonian Pacific coast of Chile. Using molecular markers, we identified both mycobionts and photobionts. The lichens, belonging to the genus Hydropunctaria and to the Wahlenbergiella group, hosted solely Ulvophycean photobionts. Pseudendoclonium submarinum (Kornmanniaceae, Ulvales) was the most common, but representatives of other closely related, yet undescribed, lineages were also found. Undulifilum symbioticum gen. et sp. nov. is described within Kornmanniaceae based on culture morphology and DNA sequence data. Furthermore, the free-living macroscopic genus Urospora (Acrosiphoniaceae, Ulotrichales) is reported as a lichen photobiont for the first time and is the first of its kind in the order. These results indicate that undescribed algal diversity is waiting to be uncovered in seashore lichens.

Botanical Garden University of Rostock Rostock Germany

Department of Botany Faculty of Science Charles University Prague Czech Republic

Zobrazit více v PubMed

Beckett, R. P., Kranner, I. & Minibayeva, F. V. 2008. Stress physiology and the symbiosis. In Nash, T. H. III [Ed.] Lichen Biology. Cambridge University Press, New York, pp. 134-51.

Binz, A. & Vischer, W. 1956. Zur Flora des Rheinlaufes bei Basel. Verhandlungen Der Naturforschenden Gesellschaft in Basel 67:195-217.

Brodo, I. M. & Slone, N. A. 2004. Lichen zonation on coastal rocks in Gwaii Haanas National Park Reserve, Haida Gwaii (Queen Charlotte Islands), British Columbia. Can. Field-nat. 118:405-24.

Castresana, J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17:540-52.

Cubero, O. F., Crespo, A., Fatehi, J. & Bridge, P. D. 1999. DNA extraction and PCR amplification method suitable for fresh, herbarium stored, lichenized, and other fungi. Plant Syst. Evol. 216:243-9.

Darienko, T. & Pröschold, T. 2017. Toward a monograph of non-marine Ulvophyceae using an integrative approach (Molecular phylogeny and systematics of terrestrial Ulvophyceae II.). Phytotaxa 324:1-41.

Darriba, T., Taboada, G. L., Doallo, R. & Posada, D. 2012. jModelTest2: more models, new heuristics and parallel computing. Nat. Methods 9:772.

DePriest, P. T. 2004. Early molecular investigations of lichen-forming symbionts: 1986-2001. Annu. Rev. Microbiol. 58:273-301.

Dobson, F. S. 2014. A Field Key to the Coastal and Seashore Lichens. Frank S. Dobson, New Malden, UK, 100 pp.

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. 8:4952.

Fletcher, A. 1973. The ecology of marine (littoral) lichens on some rocky shores of Anglesey. Lichenologist 5:368-400.

Gasulla, F., Guéra, A., de los Ríos, A. & Pérez-Ortega, S. 2019. Differential responses to salt concentrations of lichen photobiont strains isolated from lichens occuring in different littoral zones. Plant Fungal Syst. 64:149-62.

Gueidain, C., Roux, C. & Lutzoni, F. 2007. Using a multigene phylogenetic analysis to assess generic delineation and character evolution in Verrucariaceae (Verrucariales, Ascomycota). Mycol. Res. 111:1145-68.

Gueidain, C., Savić, S., Thüs, H., Roux, C., Keller, C., Tibell, L., Prieto, M. et al. 2009. Generic classification of the Verrucariaceae (Ascomycota) based on molecular and morphological evidence: recent progress and remaining challenges. Taxon 58:184-208.

Gueidain, C., Thüs, H. & Pérez-Ortega, S. 2011. Phylogenetic position of the brown algae-associated lichenized fungus Verrucaria tavaresiae (Verrucariaceae). Bryologist 114:563-9.

Hamby, R. K., Sims, L. E., Issle, L. E. & Zimme, R. E. A. 1988. Direct RNA sequencing: optimization of extraction and sequencing techniques for work with higher plants. Plant Mol. Biol. Rep. 6:179-97.

Hanic, L. A. 2005. Taxonomy, gamete morphology, and mating types of Urospora (Ulotrichales, Chlorophyta) in North America. Phycologia 44:183-93.

Hawksworth, D. L. 2000. Freshwater and marine lichen-forming fungi. In Hyde, K. D., Ho, W. H. & Pointing, S. B. [Eds.] Aquatic Mycology across the Millennium. Fungal Diversity Press, 5, pp. 1-7.

Helms, G. 2003. Taxonomy and Symbiosis in Associations of Physciaceae and Trebouxia. PhD dissertation, Univerisity of Göttingen. 156 pp.

Katoh, K., Rozewicki, J. & Yamada, K. D. 2017. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinf. 18:1e7.

Kohlmeyer, J., Hawksworth, D. L. & Volkmann-Kohlmeyer, B. 2004. Observations on two marine and maritime “borderline” lichens: Mastodia tessellata and Collemopsidium pelvetiae. Mycol. Prog. 3:51-6.

Lindstrom, S. C. & Hanic, L. A. 2005. The phylogeny of North American Urospora (Ulotrichales, Chlorophyta) based on sequence analysis of nuclear ribosomal genes, introns and spacers. Phycologia 44:194-201.

Liu, B., Wang, Q., Li, S., Fang, J., Liu, G. & Hu, Z. 2019. Taxonomic transfer of Gongrosira fluminensis Fritsch (Chaetophorales, Chlorophyceae) to Lithotrichon Darienko et Pröschold (Ulvales, Ulvophyceae) based on morphological observation and phylogenetic analyses. Fottea 19:25-32.

Miadlikowska, J., Kauff, F., Hofstetter, V., Fraker, E., Grube, M., Hafellner, J., Reeb, V. et al. 2006. New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes. Mycologia 98:1088-103.

Miller, M. A., Pfeiffer, W. & Schwartz, T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop. 2010; 14 Nov. 2010: 1-8.

Nelsen, M. P., Rivas Plata, E., Andrew, C. J., Lücking, R. & Lumbsch, H. T. 2011. Phylogenetic diversity of trentepohlialean algae associated with lichen-forming fungi. J. Phycol. 47:282-90.

Orange, A. 2012. Semi-cryptic marine species of Hydropunctaria (Verrucariaceae, lichenized Ascomycota) from north-west Europe. Lichenologist 44:299-320.

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

Parra, O. O. & Redon, J. 1977. Aislamento de Heterococcus caespitosus Vischer ficobionte de Verrucaria maura Wahlenb. Bol. Soc. Biol. Concepc. 51:219.

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. 20:3936-48.

Pérez-Ortega, S., Miller, K. A. & de los Ríos, A. 2018. Challenging the lichen concept: Turgidosculum ulvae (Verrucariaceae) represents an independent photobiont shift to a multicellular blade-like alga. Lichenologist 50:341-56.

Pérez-Ortega, S., de los Ríos, A., Crespo, A. & Sancho, L. G. 2010. Symbiotic lifestyle and phylogenetic relationships of the bionts of Mastodia tessellata (Ascomycota, incertae sedis). Am. J. Bot. 97:738-52.

R Core Team 2021. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/.

Rambaut, A. 2016. FigTree. Tree Figure Drawing Tool. University of Edinburgh, Edinburgh, UK. Available at: http://tree.bio.ed.ac.uk/.

Revell, L. J. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3:217-23.

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

Rolshausen, G., Dal Grande, F., Sadowska-Deś, A. D., Otte, J. & Schmitt, I. 2018. Quantifying the climatic niche of symbiont partners in a lichen symbiosis indicates mutualist-mediated niche expansions. Ecography 41:1380-92.

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A. & Huelsenbeck, J. P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-42.

Sanders, W. B. & Masumoto, H. 2021. Lichen algae: the photosynthetic partners in lichen symbioses. Lichenologist 53:347-93.

Sanders, W. B., Moe, R. L. & Ascaso, C. 2004. The intertidal marine lichen formed by the Pyrenomycete fungus Verrucaria tavaresiae (Ascomycotina) and the brown alga Petroderma maculiforme (Phaeophyceae): thallus organization and symbiont interaction. Am. J. Bot. 91:511-22.

Savić, S., Tibell, L., Gueidan, C. & Lutzoni, F. 2008. Molecular phylogeny and systematics of Polyblastia (Verrucariaceae, Eurotiomycetes) and allied genera. Mycol. Res. 112:1307-18.

Škaloud, P. & Rindi, F. 2013. Ecological differentiation of cryptic species within an asexual protist morphospecies: a case study of filamentous green alga Klebsormidium (Streptophyta). J. Eukaryot. Microbiol. 60:350-62.

Škaloud, P., Rindi, F., Boedeker, C. & Leliaert, F. 2018. Freshwater Flora of Central Europe, Vol 13: Chlorophyta: Ulvophyceae. Springer Spektrum, Berlin, 289 pp.

Spribille, T., Fryday, A., Pérez-Ortega, S., Svensson, M., Tønsberg, T., Ekman, S., Holien, H. et al. 2020. Lichens and associated fungi from Glacier Bay National Park, Alaska. Lichenologist 52:61-181.

Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 30:1312-3. https://doi.org/10.1093/bioinformatics/btu033.

Starr, R. C. & Zeikus, J. A. 1993. UTEX the culture collection of algae at the University of Texas at Austin. J. Phycol. Suppl. 29:1-106.

Thüs, H., Muggia, L., Pérez-Ortega, S., Favero-Longo, S. E., Joneson, S., O'Brien, H., Nelsen, M. P. et al. 2011. Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota). Eur. J. Phycol. 46:399-415.

Tschermak-Woess, E. 1976. Algal taxonomy and the taxonomy of lichens: the phycobiont of Verrucaria adriatica. In Brosn, D. H., Hawksworth, D. L. & Bailey, R. H. [Eds.] Lichenology: Progress and Problems. Academic Press, New York, pp. 79-88.

Tschermak-Woess, E. 1989. The algal partner. In Galun, M. [Ed.] CRC Handbook of Lichenology, Volume I. CRC Press, Inc, Boca Raton, Florida, pp. 39-92.

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. 27:3016-33.

Vilgalys, R. & Hester, M. 1990. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J. Bacteriol. 172:4238-46.

Watanabe, S., Nakano, T. & Deguchi, H. 1997. Photobionts from maritime lichens. J. Mar. Biotechnol. 5:103-12.

White, T. J., Bruns, T., Lee, S. & Taylor, J. W. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J. [Eds.] PCR Protocols: A Guide to Methods and Applications. Academic Press Inc, San Diego, California, pp. 315-22.

Wille, N. 1901. Studien über Chlorophyceen I-VII. Skrifter udgivne af Videnskabsselskabet i Christiania. Mathematisk-Naturvidenskaelig Klasse 6:1-46.

Zoller, S., Scheidegger, C. & Sperisen, C. 1999. PCR primers for the amplification of mitochondrial small subunit ribosomal DNA of lichen-forming Ascomycetes. Lichenologist 31:511-6.

Zwickl, D. J. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. The University of Texas, Austin.

Broad Ecological Niche in Seashore Lichens Emerges From a Stable, Selective Association With Generalist Algal Symbionts

Zobrazit více v PubMed

RefSeq
OL3429959, OL342977, OL342987, OL619283, OL342950, OL684554, OL342960, OL342978, OL342988, OL619284, OL342951, OL684555, OL342961, OL342989, OL619285, OL342962, OL342990, OL619286, OL684556, OL342963, OL619287, OL342964, OL342952, OL342965, OL619288, OL342966, OL342991, OL619289, OL342967, OL342979, OL342992, OL619290, OL342968, OL342980, OL342993, OL619291, OL342953, OL684557, OL342969, OL342994, OL619292, OL342954, OL684558, OL342970, OL342981, OL342995, OL619293, OL342955, OL342971, OL342982, OL342996, OL619294, OL342983, OL342997, OL619295, OL342972, OL342984, OL342998, OL619296, OL342956, OL684559, OL342973, OL342985, OL342999, OL619297, OL342957, OL342974, OL343000, OL619298, OL342975, OL343001, OL619299, OL342976, OL342986, OL343002, OL619300, OL342958, OL684560, OL343003, OL343004