Abstract
The genus Dermatocarpon (Verrucariaceae) is a rock-inhabiting lichen, mostly grows along the edges of lakes, rivers, streams, and watercourses. Dermatocarpon species are widely distributed from the tropics to the polar regions. In present study, D. miniatum samples were collected from the Indian Himalayas; the mycobiont and their photobionts are identified using morphological and molecular methods. The ITS rDNA markers was amplified for the DNA extracted from cultured photobiont isolates and mycobiont. The light and confocal laser scanning microscope were used for morphological evaluation of the photobionts. The nuclear ITS rDNA gene of the mycobionts and photobionts were sequenced to confirm identity. The phylogenetic trees of mycobionts and photobionts were constructed using the Maximum likelihood method that revealed an evolutionary affinity of lichen D. miniatum and photobiont Diplosphaera chodatii with similar taxa. The D. chodatii (Trebouxiophyceae) was associated with all samples of D. miniatum. This study concludes that Diplosphaera chodatii is the primary photobiont associated with D. miniatum. To the best of our knowledge this is the first study of diversity for the photobiont associated with D. miniatum from India.
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References
Amtoft A, Lutzoni F, Miadlikowska J. Dermatocarpon (Verrucariaceae) in the Ozark Highlands. North America Bryologist. 2008;111(1):1–40.
Aptroot A, Seaward M. Freshwater lichens Fungal Diversity Research Series. 2003;10:101–10.
Awasthi DD. Compendium of the Macrolichens from India. Bishen Singh Mahendra Pal Singh: Nepal and Sri Lanka; 2007.
Bast F. Sequence similarity search, multiple sequence alignment, model selection, distance matrix and phylogeny reconstruction. Protoc: Nat; 2013.
Bischoff H, Bold H. Some soil algae from enchanted rocks and related species. University of Texas Publications No. 6318. Phycol Stud. 1963;4:1–95.
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7.
Elshobary ME, Osman ME, Abushady AM, Piercey-Normore MD. Comparison of lichen-forming cyanobacterial and green algal photobionts with free-living algae. Cryptogam. Algol. 2015;36(1):81–100.
Ertz D, Guzow-Krzemińska B, Thor G, Łubek A, Kukwa M. Photobiont switching causes changes in the reproduction strategy and phenotypic dimorphism in the Arthoniomycetes. Sci Rep. 2018;8(1):1–14.
Fontaine KM, Beck A, Stocker-Wörgötter E, Piercey-Normore MD. Photobiont relationships and phylogenetic history of Dermatocarpon luridum var. luridum and related Dermatocarpon species. Plants. 2012;1(2):39–60.
Fontaine KM, Booth T, Deduke C, Piercey-Normore MD. Notes on the species assemblage of the lichen Dermatocarpon luridum in Northwestern Manitoba. Canada Evansia. 2014;31(2):69–74.
Fontaine KM, Stocker-Woergoetter E, Booth T, D Piercey-Normore M. Genetic diversity of the lichen-forming alga, Diplosphaera chodatii, in North America and Europe. Lichenologist. 2013;45(6):799.
Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. MolEcol. 1993;2(2):113–8.
Gärtner G, Ingolic E. Problems in the identification of lichen photobionts. IAL 3 - Proceedings.1998. p. 373–380.
Gasulla F, Guéra A, Barreno E. A simple and rapid method for isolating lichen photobionts. Symbiosis. 2010;51(2):175–9.
Gueidan C, Roux C, Lutzoni F. Using a multigene phylogenetic analysis to assess generic delineation and character evolution in Verrucariaceae (Verrucariales, Ascomycota). Mycol Res. 2007;111(10):1145–68.
Gueidan C, Savić S, Thüs H, Roux C, Keller C, Tibell L, et al. Generic classification of the Verrucariaceae (Ascomycota) based on molecular and morphological evidence: recent progress and remaining challenges. Taxon. 2009;58(1):184–208.
Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59(3):307–21.
Harada H. Taxonomic study on Dermatocarpon and its allied genera (Lichenes, Verrucariaceae) in Japan. Nat Hist Res. 1993;2(2):113–52.
Heiðmarsson S, Gueidan C, Miadlikowska J, Lutzoni F. Multi-locus phylogeny supports the placement of Endocarpon pulvinatum within Staurothele s. str. (Lichenised Ascomycetes, Eurotiomycetes, Verrucariaceae). Phytotaxa. 2017;306(1):037–48.
Heidmarsson S. Molecular study of Dermatocarpon miniatum (Verrucariales) and allied taxa. Mycol Res. 2003;107(4):459–68.
Heiömarsson S. The genus Dermatocarpon (Verrucariales, lichenizedAscomycotina) in the Nordic countries. Nordic Countries Nord J Bot. 2000;20(5):605–39.
Holm-Hansen C, Vainio K. Sequencing of viral genes. Molecular Epidemiology of Microorganisms. Springer; 2009. p. 203–15.
Honegger R. Lichen-forming fungi and their photobionts. Plant relationships. Springer; 2009. p. 307–33.
Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J MolEvol. 1980;16(2):111–20.
Kirk P, Cannon P, Minter D, Stalpers J. Dictionary of the fungi. CAB International. Wallingford: UK; 2008. p. 640.
Kroken S, Taylor JW. Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist. 2000;645–60.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. MolBiolEvol. 2018;35(6):1547–9.
Larena I, Salazar O, González V, Julián MaC, Rubio V. Design of a primer for ribosomal DNA internal transcribed spacer with enhanced specificity for ascomycetes. J. Biotechnol. 1999;75(2–3):187–94.
Lücking R, Hodkinson BP, Leavitt SD. The 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota-Approaching one thousand genera. Bryologist. 2017;119(4):361–416.
Molins A, García-Breijo F-J, ReigArmiñana J, Del Campo EM, Casano L, Barreno RE. Coexistence of different intrathalline symbiotic algae and bacterial biofilms in the foliose Canarian lichen Parmotrema pseudotinctorum. Vieraea Folia: ScientarumBiologicarumCanariensium. 2013;41:349–70.
Moya P, Molins A, Martínez-Alberola F, Muggia L, Barreno E. Unexpected associated microalgal diversity in the lichen Ramalina farinacea is uncovered by pyrosequencing analyses. PLoS ONE. 2017;12(4):e0175091.
Nayaka S. Methods and techniques in collection, preservation and identification of lichens. New Delhi: Plant Taxonomy and Biosystematics-Classical and Modern Methods. New India Publishing Agency; 2014. p. 101–28.
Nyati S, Beck A, Honegger R. Fine structure and phylogeny of green algal photobionts in the microfilamentous genus Psoroglaena (Verrucariaceae, lichen-forming ascomycetes). Plant Biol. 2007;9(3):390–9.
Orange A, James PW, White F. Microchemical methods for the identification of lichens. London: British Lichen Society; 2001.
Peveling E. Elektronenoptische Untersuchungen an Flechten: II. Die Feinstruktur von Trebouxia-Phycobionten. Planta. 1969:69–85.
Rai H, Khare R, Upreti DK, Ahti T. Terricolous lichens of India: taxonomic keys and description. Terricolous lichens in India. Springer; 2014. p. 17–294.
Richardson D. Photosynthesis and carbohydrate movement. The lichens. Elsevier; 1973. p. 249–88.
Shields LM, Mitchell C, Drouet F. Alga-and lichen-stabilized surface crusts as soil nitrogen sources. Am J Bot. 1957;489–98.
Shivarov VV, Denchev CM, Holger T. Ecology and distribution of Dermatocarpon (Verrucariaceae, Ascomycota) in the catchment areas of two Bulgarian rivers. Lichenologist. 2018;50(6):679–90.
Singh KP, Sinha GP. Indian lichens: an annotated checklist. Kolkata: Botanical Survey of India; 2010.
Stocker-Wôrgôtter E, Türk R. Theresynthesis of thalli of Dermatocarpon miniatum under laboratory conditions. Symbiosis. 1989;7:37–50.
Tamura K, Nei M, Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. ProcNatlAcadSci USA. 2004;101(30):11030–5.
Thüs H, Muggia L, Pérez-Ortega S, Favero-Longo SE, Joneson S, O’Brien H, et al. Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota). Eur J Phycol. 2011;46(4):399–415.
Thüs H. Taxonomie, Verbreitung und Ökologie silicoler-Süßwasserflechten im außeralpinen Mitteleuropa. Mycotaxon. 2003;87.
Tschermak-Woess E. The algal partner. In CRC handbook of lichenology. 1988;1:39–92.
Verbruggen H, Theriot EC. Building trees of algae: some advances in phylogenetic and evolutionary analysis. Eur J Phycol. 2008;43(3):229–52.
White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols Guide Methods Appl. 1990;18(1):315–22.
Acknowledgements
This study was supported by grant-in-aid from CSIR-Sponsored Research Scheme (60(0114)/17/EMR-II) awarded to FB. We are grateful to Dr. Kiran Toppo, Senior Technical Officer, Algology Laboratory, CSIR-National Botanical Research Institute, Lucknow, for providing us light microscopic images of photobionts. Figures were created with BioRender.com.
Funding
This work was supported by the Council of Scientific and Industrial Research (CSIR), New Delhi (No. 60(0114)/17/EMR-II).
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FB conceived the idea of the manuscript. KCS collected the samples, performed experiments, analyzed the data, and drafted the manuscript. AKG helped in culturing and sequencing experiments. SN helped in the morphological analysis of lichen samples and reviewed the manuscript. FB proof checked and finalized the manuscript.
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Saini, K.C., Bast, F., Nayaka, S. et al. Morpho-molecular characterization of rock-inhabiting lichen Dermatocarpon miniatum (Verrucariaceae, Ascomycota) and its symbiont in Indian Himalayas. Nucleus 64, 193–202 (2021). https://doi.org/10.1007/s13237-021-00349-0
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DOI: https://doi.org/10.1007/s13237-021-00349-0