Download PDF
Planta Med 2020; 86(13/14): 960-966
DOI: 10.1055/a-1045-1989
Biological and Pharmacological Activity
Original Papers

Endolichenic fungal diversity associated with some lichens of the Western Ghats

Meenavalli Babu Govinda Rajulu
1   Vivekananda Institute of Tropical Mycology (VINSTROM), Ramakrishna Mission Vidyapith, Chennai, India
,
Nagamani Thirunavukkarasu
2   PG & Research Department of Botany, Ramakrishna Mission Vivekananda College, Chennai, India
,
Subramanya Shravan Kumar
3   Divecha Centre for Climate Change & Centre for Ecological Sciences, Indian Institute of Science, Bangalore, India
,
Tanveer Kaur
4   Department of Biotechnology, Thapar Institute of Engineering & Technology, Patiala, Punjab, India
,
Mondem Sudhakara Reddy
4   Department of Biotechnology, Thapar Institute of Engineering & Technology, Patiala, Punjab, India
,
Trichur Subramanian Suryanarayanan
1   Vivekananda Institute of Tropical Mycology (VINSTROM), Ramakrishna Mission Vidyapith, Chennai, India
› Author AffiliationsSupported by: University Grants Commission F. MRP- 6366/16 (UGC- SERO)
› Further Information
Also available at
    Permissions and Reprints

Abstract

A total of 389 strains of fungi belonging to 38 species were isolated from 10 lichen species of the Western Ghats, southern India. All the lichens screened, irrespective of their growth forms or location, harboured endolichenic fungi. Most of the fungi belonged to the Ascomycotina. Chaetomium sp. 1, Hypoxylon investiens, Nemania bipapillata, Nodulisporium sp., Paecilomyces sp., and Sporormiella intermedia were the most common ones and were present in 5 or more lichen species. Of the 28 sporulating fungi, 7 belonged to Xylariales, and their total colonization frequency in all the lichens was also high. This observation further substantiates the high ecological amplitude of Xylariales, possibly due to overlapping ecological niches and their ability to inhibit co-occurring endolichenic fungi.

Key words

endophytic fungi - host jump - host range - microbiome - Xylaria


Publication History

Received: 04 September 2019

Accepted after revision: 05 November 2019

Article published online:
25 November 2019

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Stuttgart · New York

 

  • References

  • 1 Yuan X, Xiao S, Taylor TN. Lichen-like symbiosis 600 million years ago. Science 2005; 308: 1017-1020
    CrossrefPubMedGoogle Scholar
  • 2 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 JP. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 2016; 353: 488-492
    CrossrefPubMedGoogle Scholar
  • 3 Biosca EG, Flores R, Santander RD, Díez-Gil JL, Barreno E. Innovative approaches using lichen enriched media to improve isolation and culturability of lichen associated bacteria. PLoS One 2016; 11: e0160328
    CrossrefPubMedGoogle Scholar
  • 4 Muggia L, Fleischhacker A, Kopun T, Grube M. Extremotolerent fungi from alpine rock lichens and their phylogenetic relationships. Fungal Divers 2016; 76: 119-142
    CrossrefPubMedGoogle Scholar
  • 5 Suryanarayanan TS, Thirunavukkarasu N, Hariharan GN, Balaji P. Occurrence of nonobligate microfungi inside lichen thalli. Sydowia 2005; 57: 120-130
    PubMedGoogle Scholar
  • 6 Paranagama PA, Wijeratne EMK, Burns AM, Marron MT, Gunatilaka MK, Arnold AE, Gunatilaka AAL. Heptaketides from Corynespora sp. inhabiting the cavern beard lichen, Usnea cavernosa: first report of metabolites of an endolichenic fungus. J Nat Prod 2007; 70: 1700-1705
    CrossrefPubMedGoogle Scholar
  • 7 UʼRen JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE. Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot 2012; 99: 898-914
    CrossrefPubMedGoogle Scholar
  • 8 Suryanarayanan TS, Thirunavukkarasu N. Endolichenic fungi: the lesser known fungal associates of lichens. Mycology 2017; 8: 189-196
    CrossrefPubMedGoogle Scholar
  • 9 Kellogg JJ, Raja HA. Endolichenic fungi: a new source of rich bioactive secondary metabolites on the horizon. Phytochem Rev 2017; 16: 271-293
    CrossrefPubMedGoogle Scholar
  • 10 Suryanarayanan TS, Govinda Rajulu MB, Rajamani T, Tripathi M, Joshi Y. Endolichenic fungi in lichens of Champawat district, Uttarakhand, northern India. Mycol Prog 2017; 16: 205-211
    CrossrefPubMedGoogle Scholar
  • 11 Maduranga K, Attanayake RN, Santhirasegaram S, Weerakoon G, Paranagama PA. Molecular phylogeny and bioprospecting of endolichenic fungi (ELF) inhabiting in the lichens collected from a mangrove ecosystem in Sri Lanka. PLoS One 2018; 13: e0200711
    CrossrefPubMedGoogle Scholar
  • 12 Li YL, Zhu RX, Li G, Wang NN, Liu CY, Zhao ZT, Lou HX. Secondary metabolites from the endolichenic fungus Ophiosphaerella korrae . RSC Adv 2019; 9: 4140-4149
    CrossrefPubMedGoogle Scholar
  • 13 Sinha GP, Nayaka S, Joseph S. Additions to the checklist of Indian lichens after 2010. Cryptogam Biodiversity Assessment 2018; Special Volume. 197-206
    PubMedGoogle Scholar
  • 14 Tripathi M, Gupta RC, Joshi Y. Assessment of endolichenic fungal diversity in some forests of Kumaun Himalaya. Curr Sci 2014; 107: 745-748
    PubMedGoogle Scholar
  • 15 Tripathi M, Joshi Y. Introduction to endophytic Fungi associated with Lichens i.e. endolichenic Fungi. In: Tripathi M, Joshi Y. eds. Endolichenic Fungi: Present and Future Trends. Singapore: Springer Nature; 2019: 27-47
    CrossrefGoogle Scholar
  • 16 Yu NH, Park SY, Kim JA, Park CH, Jeong MH, Oh SO, Hong SG, Talavera M, Divakar PK, Hur JS. Endophytic and endolichenic fungal diversity in maritime Antarctica based on cultured material and their evolutionary position among Dikarya. Fungal Sys Evol 2018; 2: 263-272
    PubMedGoogle Scholar
  • 17 Zhang T, Wei XL, Zhang YQ, Liu HY, Yu LY. Diversity and distribution of lichen-associated fungi in the Ny-Ålesund Region (Svalbard, High Arctic) as revealed by 454 pyrosequencing. Sci Rep 2015; 5: 14850
    CrossrefPubMedGoogle Scholar
  • 18 Wang Y, Zheng Y, Wang X, Wei X, Wei J. Lichen-associated fungal community in Hypogymnia hypotrypa (Parmeliaceae, Ascomycota) affected by geographic distribution and altitude. Front Microbiol 2016; 7: 1231
    CrossrefPubMedGoogle Scholar
  • 19 Li WC, Zhou J, Guo SY, Guo LD. Endophytic fungi associated with lichens in Baihua mountain of Beijing, China. Fungal Divers 2007; 25: 69-80
    PubMedGoogle Scholar
  • 20 Kannangara BTSDP, Rajapaksha RSCG, Paranagama PA. Nature and bioactivities of endolichenic fungi in Pseudocyphellaria sp., Parmotrema sp. and Usnea sp. at Hakgala montane forest in Sri Lanka. Lett Appl Microbiol 2009; 48: 203-209
    CrossrefPubMedGoogle Scholar
  • 21 UʼRen JM, Lutzoni F, Miadlikowska J, Arnold AE. Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microb Ecol 2010; 60: 340-353
    CrossrefPubMedGoogle Scholar
  • 22 Chagnon PL, UʼRen JM, Miadlikowska J, Lutzoni F, Arnold AE. Interaction type influences ecological network structure more than local abiotic conditions: evidence from endophytic and endolichenic fungi at a continental scale. Oecologia 2016; 180: 181-191
    CrossrefPubMedGoogle Scholar
  • 23 UʼRen JM, Riddle JM, Monacell JT, Carbone I, Miadlikowska J, Arnold AE. Tissue storage and primer selection influence pyrosequencing-based inferences of diversity and community composition of endolichenic and endophytic fungi. Mol Ecol Res 2014; 14: 1032-1048
    PubMedGoogle Scholar
  • 24 Blaalid R, Davey ML, Kauserud H, Carlsen T, Halvorsen R, Høiland K, Eidesen PB. Arctic root-associated fungal community composition reflects environmental filtering. Mol Ecol 2014; 23: 649-659
    CrossrefPubMedGoogle Scholar
  • 25 Ko Ko TW, Stephenson SL, Bahkali AH, Hyde KD. From morphology to molecular biology: can we use sequence data to identify fungal endophytes?. Fungal Divers 2011; 50: 113-120
    CrossrefPubMedGoogle Scholar
  • 26 Okane I, Srikitikulchai P, Toyama K, Læssøe T, Sivichai S, Hywel-Jones N, Nakagiri A, Potacharoen W, Suzuki KI. Study of endophytic Xylariaceae in Thailand: diversity and taxonomy inferred from rDNA sequence analyses with saprobes forming fruit bodies in the field. Mycoscience 2008; 49: 359-372
    CrossrefPubMedGoogle Scholar
  • 27 Govinda Rajulu MB, Thirunavukkarasu N, Babu AG, Aggarwal A, Suryanarayanan TS, Reddy MS. Endophytic Xylariaceae from the forests of Western Ghats, southern India: distribution and biological activities. Mycology 2013; 4: 29-37
    PubMedGoogle Scholar
  • 28 Thomas DC, Vandergrift R, Ludden A, Carroll GC, Roy BA. Spatial ecology of the fungal genus Xylaria in a tropical cloud forest. Biotropica 2016; 48: 381-393
    CrossrefPubMedGoogle Scholar
  • 29 Rajamani T, Suryanarayanan TS, Murali TS, Thirunavukkarasu N. Distribution and diversity of foliar endophytic fungi in the mangroves of Andaman Islands, India. Fungal Ecol 2018; 36: 109-116
    CrossrefPubMedGoogle Scholar
  • 30 Suryanarayanan TS, Devarajan PT, Girivasan KP, Govinda Rajulu MB, Kumaresan V, Murali TS, Rajamani T, Thirunavukkarasu N, Venkatesan G. The host range of multi-host endophytic fungi. Curr Sci 2018; 115: 1963-1969
    CrossrefPubMedGoogle Scholar
  • 31 Davis EC, Franklin JB, Shaw AJ, Vilgalys R. Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: phylogenetics, distribution, and symbiosis. Am J Bot 2003; 90: 1661-1667
    CrossrefPubMedGoogle Scholar
  • 32 Shipunov A, Newcombe G, Raghavendra AKH, Anderson CL. Hidden diversity of endophytic fungi in an invasive plant. Am J Bot 2008; 95: 1096-1108
    CrossrefPubMedGoogle Scholar
  • 33 Thines M. An evolutionary framework for host shifts – jumping ships for survival. New Phytol 2019; DOI: 10.1111/nph.16092.
    CrossrefPubMedGoogle Scholar
  • 34 Arnold AE, Miadlikowska J, Higgins KL, Sarvate SD, Gugger P, Way A, Hofstetter V, Kauff F, Lutzoni F. A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification?. Sys Biol 2009; 58: 283-297
    CrossrefPubMedGoogle Scholar
  • 35 Nash TH. Lichen Biology. 2nd edition. Cambridge: Cambridge University Press; 2008: 1-502
    CrossrefGoogle Scholar
  • 36 Muggia L, Kopun T, Grube M. Effects of growth media on the diversity of culturable fungi from lichens. Molecules 2017; 22: 824
    CrossrefPubMedGoogle Scholar
  • 37 Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J. Biodiversity hotspots for conservation priorities. Nature 2000; 403: 853-858
    CrossrefPubMedGoogle Scholar
  • 38 Schulz B, Guske S, Dammann U, Boyle C. Endophyte-host interactions. II. Defining symbiosis of the endophyte-host interaction. Symbiosis 1998; 25: 213-227
    PubMedGoogle Scholar
  • 39 Allen GC, Flores-Vergara MA, Krasynanski S, Kumar S, Thompson WF. A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nat Protoc 2006; 1: 2320-2325
    CrossrefPubMedGoogle Scholar
  • 40 White TJ, Bruns T, Lee S, Taylor J. Amplification and direct Sequencing of fungal ribosomal RNA Genes for Phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ. eds. PCR Protocols: a Guide to Methods and Applications. San Diego: Academic Press; 1990: 315-322
    Google Scholar
  • 41 Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28: 2731-2739
    CrossrefPubMedGoogle Scholar
  • 42 Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16: 111-120
    CrossrefPubMedGoogle Scholar
  • 43 Fisher RA, Corbet AS, Williams CB. The relation between the number of species and the number of individuals in a random sample of an animal population. J Anim Ecol 1943; 12: 42-58
    CrossrefPubMedGoogle Scholar
  • 44 Suryanarayanan TS, Murali TS, Thirunavukkarasu N, Govinda Rajulu MB, Venkatesan G, Sukumar R. Endophytic fungal communities in woody perennials of three tropical forest types of the Western Ghats, southern India. Biodivers Conserv 2011; 20: 913-928
    CrossrefPubMedGoogle Scholar