Skip to main content
Log in

Morpho-molecular characterization of rock-inhabiting lichen Dermatocarpon miniatum (Verrucariaceae, Ascomycota) and its symbiont in Indian Himalayas

  • Original Article
  • Published:
The Nucleus Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Amtoft A, Lutzoni F, Miadlikowska J. Dermatocarpon (Verrucariaceae) in the Ozark Highlands. North America Bryologist. 2008;111(1):1–40.

    Google Scholar 

  2. Aptroot A, Seaward M. Freshwater lichens Fungal Diversity Research Series. 2003;10:101–10.

    Google Scholar 

  3. Awasthi DD. Compendium of the Macrolichens from India. Bishen Singh Mahendra Pal Singh: Nepal and Sri Lanka; 2007.

    Google Scholar 

  4. Bast F. Sequence similarity search, multiple sequence alignment, model selection, distance matrix and phylogeny reconstruction. Protoc: Nat; 2013.

    Book  Google Scholar 

  5. 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.

  6. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7.

    Article  CAS  Google Scholar 

  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.

  8. 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.

    Article  CAS  Google Scholar 

  9. 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.

  10. 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.

    Article  Google Scholar 

  11. 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.

  12. 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.

    CAS  Google Scholar 

  13. Gärtner G, Ingolic E. Problems in the identification of lichen photobionts. IAL 3 - Proceedings.1998. p. 373–380.

  14. Gasulla F, Guéra A, Barreno E. A simple and rapid method for isolating lichen photobionts. Symbiosis. 2010;51(2):175–9.

    Article  Google Scholar 

  15. 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.

    Article  CAS  Google Scholar 

  16. 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.

    Article  Google Scholar 

  17. 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.

  18. Harada H. Taxonomic study on Dermatocarpon and its allied genera (Lichenes, Verrucariaceae) in Japan. Nat Hist Res. 1993;2(2):113–52.

    Google Scholar 

  19. 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.

  20. Heidmarsson S. Molecular study of Dermatocarpon miniatum (Verrucariales) and allied taxa. Mycol Res. 2003;107(4):459–68.

    Article  Google Scholar 

  21. Heiömarsson S. The genus Dermatocarpon (Verrucariales, lichenizedAscomycotina) in the Nordic countries. Nordic Countries Nord J Bot. 2000;20(5):605–39.

    Article  Google Scholar 

  22. Holm-Hansen C, Vainio K. Sequencing of viral genes. Molecular Epidemiology of Microorganisms. Springer; 2009. p. 203–15.

  23. Honegger R. Lichen-forming fungi and their photobionts. Plant relationships. Springer; 2009. p. 307–33.

  24. 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.

    CAS  Google Scholar 

  25. Kirk P, Cannon P, Minter D, Stalpers J. Dictionary of the fungi. CAB International. Wallingford: UK; 2008. p. 640.

    Google Scholar 

  26. 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.

  27. 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.

    CAS  Google Scholar 

  28. 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.

  29. 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.

    Article  Google Scholar 

  30. 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.

    Google Scholar 

  31. 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.

    Article  Google Scholar 

  32. 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.

    Google Scholar 

  33. 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.

    Article  CAS  Google Scholar 

  34. Orange A, James PW, White F. Microchemical methods for the identification of lichens. London: British Lichen Society; 2001.

    Google Scholar 

  35. Peveling E. Elektronenoptische Untersuchungen an Flechten: II. Die Feinstruktur von Trebouxia-Phycobionten. Planta. 1969:69–85.

  36. 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.

  37. Richardson D. Photosynthesis and carbohydrate movement. The lichens. Elsevier; 1973. p. 249–88.

  38. Shields LM, Mitchell C, Drouet F. Alga-and lichen-stabilized surface crusts as soil nitrogen sources. Am J Bot. 1957;489–98.

  39. 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.

    Article  Google Scholar 

  40. Singh KP, Sinha GP. Indian lichens: an annotated checklist. Kolkata: Botanical Survey of India; 2010.

    Google Scholar 

  41. Stocker-Wôrgôtter E, Türk R. Theresynthesis of thalli of Dermatocarpon miniatum under laboratory conditions. Symbiosis. 1989;7:37–50.

    Google Scholar 

  42. 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.

    Article  CAS  Google Scholar 

  43. 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.

    Article  Google Scholar 

  44. Thüs H. Taxonomie, Verbreitung und Ökologie silicoler-Süßwasserflechten im außeralpinen Mitteleuropa. Mycotaxon. 2003;87.

  45. Tschermak-Woess E. The algal partner. In CRC handbook of lichenology. 1988;1:39–92.

    Google Scholar 

  46. Verbruggen H, Theriot EC. Building trees of algae: some advances in phylogenetic and evolutionary analysis. Eur J Phycol. 2008;43(3):229–52.

    Article  Google Scholar 

  47. 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.

    Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Felix Bast.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Corresponding Editor: Amita Pal; Reviewers: TAM Jagdeesh Ram, Krishna Pal Singh.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13237-021-00349-0

Keywords

Navigation