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Assessment of fungal diversity present in lakes of Maritime Antarctica using DNA metabarcoding: a temporal microcosm experiment

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Abstract

We evaluated the fungal diversity in two lakes on the South Shetland Islands, using DNA metabarcoding through high-throughput sequencing (HTS). A microcosm experiment was deployed for two consecutive years in lakes on Deception and King George islands to capture potential decomposer freshwater fungi. Analyses of the baits revealed 258,326 DNA reads distributed in 34 fungal taxa of the phyla Ascomycota, Basidiomycota, Mortierellomycota, Chytridiomycota and Rozellomycota. Tetracladium marchalianum, Tetracladium sp., Rozellomycota sp., Fungal sp. 1 and Fungal sp. 2 were the most common taxa detected. However, the majority of the communities comprised intermediate and rare taxa. Both fungal communities displayed moderate indices of diversity, richness and dominance. Only six taxa were detected in both lakes, including the most dominant T. marchalianum and Tetracladium sp. The high numbers of reads of the known aquatic saprotrophic hyphomycetes T. marchalianum and Tetracladium sp. in the baits suggest that these fungi may digest organic material in Antarctic lakes, releasing available carbon and nutrients to the other aquatic organisms present in the complex lake food web. Our data confirm that the use of cotton baits together with HTS approaches can be appropriate to study the diversity of resident freshwater fungi present in Antarctic lakes.

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References

  • Abarenkov K, Zirk A, Piirmann T et al (2020) UNITE QIIME release for eukaryotes. Version 04.02.2020. UNITE Community

  • Abdel-Raheem A, Ali E (2004) Lignocellulolytic enzyme production by aquatic hyphomycetes species isolated from the Nile’s Delta region. Mycopathologia 157:277–286

    CAS  PubMed  Google Scholar 

  • Anderson JL, Shearer CA (2011) Population genetics of the aquatic fungus Tetracladium marchalianum over space and time. PLoS ONE 6:e15908

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bardou P, Mariette J, Escudié F et al (2014) An interactive Venn diagram viewer. BMC Bioinform 15:293

    Google Scholar 

  • Bärlocher F (1992) Research on aquatic hyphomycetes: historical background and overview. In: Bärlocher F (ed) The ecology of aquatic hyphomycetes. Springer Verlag, Berlin, pp 1–15

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bridge PD, Spooner BM (2012) Non-lichenized Antarctic fungi: transient visitors or members of a cryptic ecosystem? Fungal Ecol 5:381–394

    Google Scholar 

  • Brunati M, Rojas JL, Sponga F et al (2009) Diversity and pharmaceutical screening of fungi from benthic mats of Antarctic lakes. Mar Genomics 2:43–50

    PubMed  Google Scholar 

  • Callahan BJ, McMurdie PJ, Rosen M et al (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat methods 13:581–583

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carvalho CR, Ferreira MC, Gonçalves VN et al (2020) Cultivable fungi associated with bryosphere of bipolar mosses Polytrichastrum alpinum and Polytrichum juniperinum in King George Island, South Shetland Islands, Maritime Antarctica. Polar Biol 43:545–553

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Connell L, Segee B, Redman R et al (2018) Biodiversity and abundance of cultured microfungi from the permanently ice-covered Lake Fryxell, Antarctica. Life 8:1–10

    CAS  Google Scholar 

  • Crous PW, Gams W, Stalpers JA et al (2004) MycoBank: an online initiative to launch mycology into the 21st century. Stud Mycol 50:19–22

    Google Scholar 

  • de Hoog GS, Göttlich E, Platas G et al (2005) Evolution, taxonomy and ecology of the genus Thelebolus in Antarctica. Stud Mycol 51:33–76

    Google Scholar 

  • Deiner K, Bik HM, Mächler E et al (2017) Environmental DNA metabarcoding: transforming how we survey animal and plant communities. Mol Ecol 26:5872–5895

    PubMed  Google Scholar 

  • Ellis-Evans JC (1985) Fungi from maritime Antarctic freshwater environments. Br Antarct Surv Bull 68:37–45

    Google Scholar 

  • Ellis-Evans JC (1996) Microbial diversity and function in Antarctic freshwater ecosystems. Biodivers Conserv 5:1395–1431

    Google Scholar 

  • Fiuza PO, PÉREZ TC, Gulis V et al (2017) Ingoldian fungi of Brazil: some new records and a review including a checklist and a key. Phytotaxa 306:171–200

    Google Scholar 

  • Giner CR, Forn I, Romac S et al (2016) Environmental sequencing provides reasonable estimates of the relative abundance of specific picoeukaryotes. Appl Environ Microbiol 82:4757–4766

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  • Hammer Ø, Harper DA, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  • He F, Lin B, Sun JZ et al (2013) Knufia aspidiotus sp. nov., a new black yeast from scale insects. Phytotaxa 153:39–50

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Izaguirre I, Mataloni G, Vinocur A et al (1993) Temporal and spatial variations of phytoplankton from Boeckella Lake (Hope Bay, Antarctic Peninsula). Antarct Sci 5:137–141

    Google Scholar 

  • 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 1 Oct 2020

  • Karling JS (2018) Tetracladium marchalianum and its relation to Asterothrix, Phycastrum, and Cerasterias. Mycology 27:478–495

    Google Scholar 

  • Kirk PM, Cannon PF, Minter DW et al (2011) Dictionary of the Fungi, 10th edn. CAB International, Wallingford

    Google Scholar 

  • Kobayasi Y (1967) Mycological studies of the Alaskan Arctic. Annu Rep Inst Ferment Osaka 3:1–138

    Google Scholar 

  • Letcher PM, Powell MJ, Davis WJ (2015) A new family and four new genera in Rhizophydiales (Chytridiomycota). Mycologia 107:808–830

    CAS  PubMed  Google Scholar 

  • Lindsey B, Glover BJ (1976) Ecological studies of spores of aquatic hyphomycetes in the cringle brook, Lincs. Hydrobiologia 5:201–208

    Google Scholar 

  • Martorell MM, Ruberto LAM, de Figueroa LIC et al (2019) Antarctic yeasts as a source of enzymes for biotechnological applications. In: Rosa LH (ed) Fungi of Antarctica: diversity, ecology and biotechnological applications. Springer, Switzerland, pp 285–304

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Montemartini A, Caretta G, Del Frate G (1993) Notes on Thelebolus microsporus isolated in Antarctica. Mycotaxon 48:343–358

    Google Scholar 

  • Ogaki MB, Vieira R, Lírio JM et al (2019) Diversity and ecology of fungal assemblages present in lakes of Antarctica. In: Rosa LH (ed) Fungi of Antarctica: diversity, ecology and biotechnological applications. Springer, Switzerland, pp 69–97

    Google Scholar 

  • Ogaki MB, Vieira R, Muniz MC et al (2020) Diversity, ecology, and bioprospecting of culturable fungi in lakes impacted by anthropogenic activities in Maritime Antarctica. Extremophiles 24:637–655

    CAS  PubMed  Google Scholar 

  • Page KA, Flannery MK (2018) Chytrid fungi associated with pollen decomposition in Crater Lake, Oregon. Fine Focus 4:83–100

    Google Scholar 

  • Quayle WC, Peck LS, Peat H et al (2002) Extreme responses to climate change in Antarctic lakes. Science 295:645–646

    CAS  PubMed  Google Scholar 

  • Quayle WC, Convey P, Peck LS et al (2003) Ecological responses of maritime Antarctic lakes to regional climate change. Antarct Res Ser 79:159–170

    Google Scholar 

  • Quesada A, Camacho A, Rochera C et al (2009) Byers Peninsula: a reference site for coastal, terrestrial and limnetic ecosystem studies in maritime Antarctica. Polar Sci 3:181–187

    Google Scholar 

  • Réblová M, Untereiner WA, Réblová K (2013) Novel evolutionary lineages revealed in the chaetothyriales (fungi) based on multigene phylogenetic analyses and comparison of its secondary structure. PLoS ONE 8:e63547

    PubMed  PubMed Central  Google Scholar 

  • Richardson RT, Lin CH, Sponsler DB et al (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 

  • Rochera C, Quesada A, Toro M et al (2017) Plankton assembly in an ultra-oligotrophic Antarctic lake over the summer transition from the ice-cover to ice-free period: a size spectra approach. Polar Sci 11:72–82

    Google Scholar 

  • Rojas-Jimenez K, Wurzbacher C, Bourne EC et al (2017) Early diverging lineages within Cryptomycota and Chytridiomycota dominate the fungal communities in ice-covered lakes of the McMurdo Dry Valleys, Antarctica. Sci Rep 7:15348

    PubMed  PubMed Central  Google Scholar 

  • Rosa LH, Zani CL, Cantrell CL et al (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. Springer, Switzerland, pp 1–18

    Google Scholar 

  • Rosa LH, da Silva TH, Ogaki MB et al (2020a) DNA metabarcoding uncovers fungal diversity in soils of protected and non-protected areas on Deception Island, Antarctica. Sci Rep 10:21986

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosa LH, de Sousa JRP, de Menezes GCA et al (2020b) Opportunistic fungal assemblages present on fairy rings spread on different moss species in the Antarctic Peninsula. Polar Biol 43:587–596

    Google Scholar 

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

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ruisi S, Barreca D, Selbmann L et al (2007) Fungi in Antarctica. Rev Environ Sci Biotechnol 6:127–141

    Google Scholar 

  • Suberkropp K (2001) Fungal growth, production, and sporulation during leaf decomposition in two streams. Appl Environ Microb 67:5063–5068

    CAS  Google Scholar 

  • Tedersoo L, Sánchez-Ramírez S, Kõljalg U et al (2018) High-level classification of the Fungi and a tool for evolutionary ecological analyses. Fungal Div 90:135–159

    Google Scholar 

  • Tsuji M, Fujiu S, Xiao N et al (2013) Cold adaptation of fungi obtained from soil and lake sediment in the Skarvsnes ice-free area, Antarctica. FEMS Microbiol Lett 346:121–130

    CAS  PubMed  Google Scholar 

  • Vincent WF (2000) Evolutionary origins of Antarctic microbiota: invasion, selection and endemism. Antarc Sci 12:374–385

    Google Scholar 

  • Walter J, Hermann V (2012) Phylogenetic relationships of five genera of Xylariales and Rosasphaeria gen. nov. (Hypocreales). Fungal Div 52:75–98

    Google Scholar 

  • Weber AA, Pawlowski J (2013) Can abundance of protists be inferred from sequence data: a case study of Foraminifera. PLoS ONE 8:e56739

    CAS  PubMed  PubMed Central  Google Scholar 

  • White TJ et al (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. Academic Press, Cambridge, pp 315–322

    Google Scholar 

  • Wong MKM, Goh TK, Hodgkiss IJ et al (1998) Role of fungi in freshwater ecosystems. Biodivires Conserv 7:1187–1206

    Google Scholar 

  • Zúñiga C, Leiva D, Ramírez-Fernández L et al (2015) Phylogenetic diversity of Peltigera cyanolichens and their photobionts in southern Chile and Antarctica. Microbes Environ 30:172–179

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study received financial support from CNPq, PROANTAR, FAPEMIG, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES), INCT Criosfera 2. P. Convey is supported by NERC core funding to the British Antarctic Survey’s ‘Biodiversity, Evolution and Adaptation’ Team. We also thank congresswoman Jô Moraes and the Biological Sciences Institute of the University of Brasilia.

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Correspondence to Luiz H. Rosa.

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Communicated by A. Oren.

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de Souza, L.M.D., Ogaki, M.B., Câmara, P.E.A.S. et al. Assessment of fungal diversity present in lakes of Maritime Antarctica using DNA metabarcoding: a temporal microcosm experiment. Extremophiles 25, 77–84 (2021). https://doi.org/10.1007/s00792-020-01212-x

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