Skip to main content

Advertisement

Log in

Fungi in the Antarctic Cryosphere: Using DNA Metabarcoding to Reveal Fungal Diversity in Glacial Ice from the Antarctic Peninsula Region

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

We assessed fungal diversity present in glacial from the Antarctic Peninsula using DNA metabarcoding through high-throughput sequencing (HTS). We detected a total of 353,879 fungal DNA reads, representing 94 genera and 184 taxa, in glacial ice fragments obtained from seven sites in the north-west Antarctic Peninsula and South Shetland Islands. The phylum Ascomycota dominated the sequence diversity, followed by Basidiomycota and Mortierellomycota. Penicillium sp., Cladosporium sp., Penicillium atrovenetum, Epicoccum nigrum, Pseudogymnoascus sp. 1, Pseudogymnoascus sp. 2, Phaeosphaeriaceae sp. and Xylaria grammica were the most dominant taxa, respectively. However, the majority of the fungal diversity comprised taxa of rare and intermediate relative abundance, predominately known mesophilic fungi. High indices of diversity and richness were calculated, along with moderate index of dominance, which varied among the different sampling sites. Only 26 (14%) of the total fungal taxa detected were present at all sampling sites. The identified diversity was dominated by saprophytic taxa, followed by known plant and animal pathogens and a low number of symbiotic fungi. Our data suggest that Antarctic glacial ice may represent a hotspot of previously unreported fungal diversity; however, further studies are required to integrate HTS and culture approaches to confirm viability of the taxa detected.

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

Similar content being viewed by others

Data Availability

All raw sequences have been deposited in the NCBI database under the codes SRX9966699, SRX9966700, SRX9966701, SRX9966702, SRX9966703, SRX9966704, SRX9966705, and SRX9966706.

References

  1. Convey P (2017) Antarctic ecosystems. In: Reference module in life sciences. Elsevier, pp 179–188. https://doi.org/10.1016/B978-0-12-809633-8.02182-8

  2. Perini L, Gostinčar C, Gunde-Cimerman N (2019) Fungal and bacterial diversity of Svalbard subglacial ice. Sci Rep 9:20230

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Rosa LH, Zani CL, Cantrell CL, Duke SO, Van Dijck P, Desideri A, Rosa CA (2019) Fungi in Antarctica: diversity, ecology, effects of climate change, and bioprospection for bioactive compounds. In: Rosa LH (ed) Fungi of Antarctica: diversity, ecology and biotechnological applications, 1st edn. Springer, Switzerland, pp 1–17. https://doi.org/10.1007/978-3-030-18367-7_1

    Chapter  Google Scholar 

  4. Anesio AM, Laybourn-Parry J (2012) Glaciers and ice sheets as a biome. Trends Ecol Evol 27:219–225

    PubMed  Google Scholar 

  5. de Menezes GCA, Porto BA, Simões JC, Rosa CA, Rosa LH (2019) Fungi in snow and glacial ice of Antarctica. In: Rosa LH (ed) Fungi of Antarctica: diversity, ecology and biotechnological applications, 1st edn. Springer, Switzerland, Cham, pp 127–146

    Google Scholar 

  6. Margesin R, Collins T (2019) Microbial ecology of the cryosphere (glacial and permafrost habitats): current knowledge. Appl Microbiol Biotech 103:2537–2549

    CAS  Google Scholar 

  7. Jacobs PH, Taylor HC, Shafer JC (1964) Studies of fungi at Amundsen-Scott IGY South Pole Base (1957). Arch Dermatol 89:117–123

    CAS  PubMed  Google Scholar 

  8. Abyzov SS, Hoover RB, Imura S, Mitskevich IN et al (2004) Use of different methods for discovery of ice-entrapped microorganisms in ancient layers of the Antarctic glacier. Adv Space Res 33:1222–1230

    Google Scholar 

  9. D’Elia T, Veerapaneni R, Theraisnathan V, Rogers SO (2009) Isolation of fungi from Lake Vostok accretion ice. Mycologia 101:751–763

    PubMed  Google Scholar 

  10. Knowlton C, Veerapaneni R, D’Elia T, Rogers SO (2013) Microbial analyses of ancient ice core sections from Greenland and Antarctica. Biology 2:206–232

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Sanyal A, Antony R, Samui G, Thamban M (2018) Microbial communities and their potential for degradation of dissolved organic carbon in cryoconite hole environments of Himalaya and Antarctica. Microbiol Res 208:32–42

    CAS  PubMed  Google Scholar 

  12. de Menezes GCA, Porto BA, Amorim SS (2020) Fungi in glacial ice of Antarctica: diversity, distribution and bioprospecting of bioactive compounds. Extremophiles 24:367–376

    PubMed  Google Scholar 

  13. Abyzov SS (1993) Microorganisms in the Antarctic ice. In: Friedman EI (ed) Antarctic microbiology. Wiley, New York, pp 265–295

    Google Scholar 

  14. Gunde-Cimerman N, Sonjak S, Zalar P (2003) Extremophilic fungi in arctic ice: a relationship between adaptation to low temperature and water activity. Phys Chem Earth, Parts A/B/C 28:1273–1278

    Google Scholar 

  15. Sonjak S, Frisvad JC, Gunde-Cimerman N (2006) Penicillium mycobiota in Arctic subglacial ice. Microb Ecol 52:207–216

    PubMed  Google Scholar 

  16. Rosa LH, Pinto OHB, Šantl-Temkiv T (2020) DNA metabarcoding of fungal diversity in air and snow of Livingston Island, South Shetland Islands. Antarctica Sci Rep 10:21793

    CAS  PubMed  Google Scholar 

  17. Rogers SO, Theraisnathan V, Ma LJ (2004) Comparisons of protocols for decontamination of environmental ice samples for biological and molecular examinations. Appl Environ Microbiol 70:2540–2544

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Chen S, Yao H, Han J et al (2010) Validation of the ITS2 region as a novel DNA barcode for identifying medicinal plant species. PLoS ONE 5:e8613. https://doi.org/10.1371/journal.pone.0008613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Richardson RT, Lin CH, Sponsler DB (2015) Application of ITS2 metabarcoding to determine the provenance of pollen collected by honey bees in an agroecosystem. Appl Plant Sci 3:1400066

    Google Scholar 

  20. White TJ, Bruns T, Lee S, Taylor J (1990) 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, 1st edn. Academic Press, New York, pp 315–322

    Google Scholar 

  21. Joshi NA, Fass JN (2011) Sickle: a sliding-window, adaptive, quality-based trimming tool for FastQ files (version 1.33) [software]. https://github.com/najoshi/sickle. Accessed 10 Aug 2020

  22. Bolyen E, Rideout JR, Dillon MR et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bokulich NA, Kaehler BD, Rideout JR et al (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6:90. https://doi.org/10.1186/s40168-018-0470-z

    Article  PubMed  PubMed Central  Google Scholar 

  25. Abarenkov, K. Zirk A, Piirmann T, Pöhönen R, Ivanov F, Nilsson RH, Kõljalg U (2020) UNITE QIIME release for eukaryotes. Version 04.02.2020. UNITE Community. https://doi.org/10.15156/BIO/786386

  26. Kirk PM, Cannon PF, Minter DW et al (2011) Dictionary of the fungi. CAB International, Wallingford

    Google Scholar 

  27. Tedersoo L, Sánchez-Ramírez S, Kõljalg U et al (2018) High-level classification of the fungi and a tool for evolutionary ecological analyses. Fungal Divers 90:135–159. https://doi.org/10.1007/s13225-018-0401-0

    Article  Google Scholar 

  28. Rosa LH, Pinto OHB, Convey P et al (2020) DNA metabarcoding to assess the diversity of airborne fungi present in air over Keller Peninsula, King George Island, Antarctica. Microb Ecol. https://doi.org/10.1007/s00248-020-01627-1

    Article  PubMed  Google Scholar 

  29. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  30. Ondov BD, Bergman NH, Phillippy AM (2011) Interactive metagenomic visualization in a Web browser. BMC Bioinformatics 12:385. https://doi.org/10.1186/1471-2105-12-385

    Article  PubMed  PubMed Central  Google Scholar 

  31. Nguyen NH, Song Z, Bates ST et al (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006

    Article  Google Scholar 

  32. Duo Saito RA, Connell L, Rodriguez R, Redman R, Libkind D, de Garcia V (2018) Metabarcoding analysis of the fungal biodiversity associated with Castaño Overa Glacier – Mount Tronador, Patagonia, Argentina. Fungal Ecol 36:8–16

    Google Scholar 

  33. Medinger R, Nolte V, Pandey RV et al (2010) Diversity in a hidden world: potential and limitation of next-generation sequencing for surveys of molecular diversity of eukaryotic microorganisms. Mol Ecol 19:32–40. https://doi.org/10.1111/j.1365-294X.2009.04478.x

    Article  PubMed  PubMed Central  Google Scholar 

  34. Weber AA, Pawlowski J (2013) Can abundance of protists be inferred from sequence data: a case study of Foraminifera. PLoS ONE 8:e56739. https://doi.org/10.1371/journal.pone.0056739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Giner CR, Forn I, Romac S, Logares RC, Massana R (2016) Environmental sequencing provides reasonable estimates of the relative abundance of specific picoeukaryotes. Appl Environ Microbiol 82:4757–4766. https://doi.org/10.1128/AEM.00560-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Deiner K, Bik HM, Mächler E et al (2017) Environmental DNA metabarcoding: transforming how we survey animal and plant communities. Mol Ecol 21:5872–5895. https://doi.org/10.1111/mec.14350

    Article  Google Scholar 

  37. Hering D, Borja A, Jones JI et al (2018) Implementation options for DNA-based identification into ecological status assessment under the European Water Framework Directive. Water Res 138:192–205. https://doi.org/10.1016/j.watres.2018.03.003

    Article  CAS  PubMed  Google Scholar 

  38. McRae CF, Hocking AD, Seppelt RD (1999) Penicillium species from terrestrial habitats in the Windmill Islands, East Antarctica, including a new species, Penicillium antarcticum. Polar Biol 21:97–111

    Google Scholar 

  39. Godinho VM, Gonçalves VN, Santiago IF et al (2015) Diversity and bioprospection of fungal community present in oligotrophic soil of continental Antarctica. Extremophiles 19:585–596. https://doi.org/10.1007/s00792-015-0741-6

    Article  PubMed  Google Scholar 

  40. Gomes EC, Godinho VM, Silva DA (2018) Cultivable fungi present in Antarctic soils: taxonomy, phylogeny, diversity, and bioprospecting of antiparasitic and herbicidal metabolites. Extremophiles 22:381–393

    CAS  PubMed  Google Scholar 

  41. Zucconi L, Selbmann L, Buzzini P (2012) Searching for eukaryotic life preserved in Antarctic permafrost. Polar Biol 35:749–757

    Google Scholar 

  42. da Silva TH, Silva DAS, de Oliveira FS (2020) Diversity, distribution, and ecology of viable fungi in permafrost and active layer of Maritime Antarctica. Extremophiles 24:565–576

    PubMed  Google Scholar 

  43. Godinho VM, Furbino LE, Santiago IF et al (2013) Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. ISME J 7:1434–1451

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Godinho VM, de Paula MTR, Silva DAS et al (2019) Diversity and distribution of hidden cultivable fungi associated with marine animals of Antarctica. Fungal Biol 123:507–516

    PubMed  Google Scholar 

  45. Gonçalves VN, Vaz AB, Rosa CA, Rosa LH (2012) Diversity and distribution of fungal communities in lakes of Antarctica. FEMS Microbiol Ecol 82:459–471

    PubMed  Google Scholar 

  46. Ogaki MB, Teixeira DR, Vieira R (2020) Diversity and bioprospecting of cultivable fungal assemblages in sediments of lakes in the Antarctic Peninsula. Fungal Biol 124:601–611

    CAS  PubMed  Google Scholar 

  47. Gonçalves VN, Vitoreli GA, de Menezes GC (2017) Taxonomy, phylogeny and ecology of cultivable fungi present in seawater gradients across the Northern Antarctica Peninsula. Extremophiles 21:1005–1015

    PubMed  Google Scholar 

  48. de Menezes GCA, Câmara PEAS, Pinto OHB (2021) Fungal diversity present on rocks from a polar desert in continental Antarctica assessed using DNA metabarcoding. Extremophiles 25:193–202

    PubMed  Google Scholar 

  49. Mercantini R, Marsella R, Cervellati MC (1989) Keratinophilic fungi isolated from Antarctic soil. Mycopathologia 106:47–52

    CAS  PubMed  Google Scholar 

  50. Lorch JM, Lindner DL, Gargas A et al (2013) A culture-based survey of fungi in soil from bat hibernacula in the eastern United States and its implications for detection of Geomyces destructans, the causal agent of bat white-nose syndrome. Mycologia 105:237–252

    CAS  PubMed  Google Scholar 

  51. Minnis AM, Lindner DL (2013) Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol 117:638–649

    PubMed  Google Scholar 

  52. Ali SH, Alias SA, Siang HY et al (2014) Studies on diversity of soil microfungi in the Hornsund area, Spitsbergen. Polar Res 35:203–224

    Google Scholar 

  53. Arenz BE, Blanchette RA (2011) Distribution and abundance of soil fungi in Antarctica at sites on the Peninsula, Ross Sea Region and McMurdo Dry Valleys. Soil Biol Biochem 43:308–315. https://doi.org/10.1016/j.soilbio.2010.10.016

    Article  CAS  Google Scholar 

  54. Krishnan A, Alias SA, Wong CMVL et al (2011) Extracellular hydrolase enzyme production by soil fungi from King George Island, Antarctica. Polar Biol 34:1535–1542

    Google Scholar 

  55. Tosi S, Casado B, Gerdol R, Caretta G (2002) Fungi isolated from Antarctic mosses. Polar Biol 25:262–268

    Google Scholar 

  56. Rosa LH, Almeida Vieira MDL, Santiago IF, Rosa CA (2010) Endophytic fungi community associated with the dicotyledonous plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) in Antarctica. FEMS Microbiol Ecol 73:178–189

    CAS  PubMed  Google Scholar 

  57. Carvalho CR, Ferreira MC, Gonçalves VN et al (2020) Fungi associated with the briosphere of the bipolar mosses Polytrichastrum alpinum and Polytrichum juniperinum in Antarctica. Polar Biol 43:545–553. https://doi.org/10.1007/s00300-020-02658-7

    Article  Google Scholar 

  58. Loque CP, Medeiros AO, Pellizzari FM et al (2010) Fungal community associated with marine macroalgae from Antarctica. Polar Biol 33:641–648

    Google Scholar 

  59. Santiago IF, Soares MA, Rosa CA, Rosa LH (2015) Lichensphere: a protected natural microhabitat of the non-lichenised fungal communities living in extreme environments of Antarctica. Extremophiles 19:1087–1097

    PubMed  Google Scholar 

  60. Rosa LH, da Silva TH, Ogaki MB et al (2020) DNA metabarcoding high-throughput sequencing uncovers cryptic fungal diversity in soils of protected and non-protected areas on Deception Island. Antarctica Sci Rep 10:21986. https://doi.org/10.1038/s41598-020-78934-7

    Article  CAS  PubMed  Google Scholar 

  61. Braga RM, Padilla G, Araújo WL (2018) The biotechnological potential of Epicoccum spp.: diversity of secondary metabolites. Crit Rev Microbiol 44:759–778

    CAS  PubMed  Google Scholar 

  62. Marshall WA (1997) Seasonality in Antarctic airborne fungal spores. Appl Environ Microbiol 63:2240–2245

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Henríquez M, Vergara K, Norambuena J (2014) Diversity of cultivable fungi associated with Antarctic marine sponges and screening for their antimicrobial, antitumoral and antioxidant potential. World J Microbiol Biotechnol 30:65–76

    PubMed  Google Scholar 

  64. Becker K, Stadler M (2020) Recent progress in biodiversity research on the Xylariales and their secondary metabolism. J Antibiot 74:1–23

    Google Scholar 

  65. Daranagama DA, Hyde KD, Sir EB et al (2018) Towards a natural classification and backbone tree for Graphostromataceae, Hypoxylaceae, Lopadostomataceae and Xylariaceae. Fungal Divers 88:1–165

    Google Scholar 

  66. Rogers JD (2000) Thoughts and musings on tropical Xylariaceae. Mycol Res 104:1412–1420

    Google Scholar 

  67. Davis EC, Franklin JB, Shaw AJ et al (2003) Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: phylogenetics, distribution, and symbiosis. Am J Bot 90:1661–1667

    PubMed  Google Scholar 

  68. Santos JAD, Meyer E, Sette LD (2020) Fungal community in Antarctic soil along the retreating Collins Glacier (Fildes Peninsula, King George Island). Microorganisms 8:1145

    PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful for the generous support of MSc. Rodrigo Paidano Alves in preparation of Fig. 1. We also thank congresswoman Jô Moraes and the Biological Sciences Institute of the University of Brasilia

Funding

We acknowledge financial support from PROANTAR CNPq (442258/2018–6), INCT Criosfera, FAPEMIG, CAPES, and FNDCT. GCA de Menezes’ scholarship was supported by CNPq (151195/2019–6). P. Convey is supported by NERC core funding to the British Antarctic Survey’s “Biodiversity, Evolution and Adaptation” Team.

Author information

Authors and Affiliations

Authors

Contributions

GCAM, LHR, JCS, and PEASC conceived the study. GCAM and LHR performed fungal DNA extraction from ice. GCAM, LHR, PEASC, OHBZ, PC, MCS, JCS, and CAR analyzed the results and wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Luiz Henrique Rosa.

Ethics declarations

Ethics Approval

The collections and studies performed in Antarctic Peninsula were authorized by the Secretariat of the Antarctic Treaty and by PROANTAR.

Conflict of Interest

The authors declare no competing interests.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Menezes, G.C.A., Câmara, P.E.A.S., Pinto, O.H.B. et al. Fungi in the Antarctic Cryosphere: Using DNA Metabarcoding to Reveal Fungal Diversity in Glacial Ice from the Antarctic Peninsula Region. Microb Ecol 83, 647–657 (2022). https://doi.org/10.1007/s00248-021-01792-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-021-01792-x

Keywords

Navigation