DNA metabarcoding of non-fungal eukaryotic diversity in air and snow of Livingston Island, South Shetland Islands, Antarctica

  • Paulo E.A.S. Câmara Departamento de Botânica, Universidade de Brasília, Brasília, Brazil; and Pós Graduação em Fungos, Algas e Plantas, Universidade Federal de Santa Catarina, Florianopolis, Brazil
  • Tina Šantl‑Temkiv Department of Biology, Aarhus University, Aarhus, Denmark; Stellar Astrophysics Centre, Department of Physics and Astronomy, Aarhus University, Aarhus, Denmark; Department of Biology, Aarhus University, Arctic Research Centre, Aarhus, Denmark; and Department of Environmental Science, iCLIMATE Aarhus University Interdisciplinary Centre for Climate Change, Aarhus University, Roskilde, Denmark
  • Otavio H.P. Pinto Departamento de Biologia Celular, Universidade de Brasília, Brasília, Brazil
  • Peter Convey British Antarctic Survey, Natural Environment Research Council, High Cross, Cambridge, UK; Department of Zoology, University of Johannesburg, Auckland Park, South Africa; and Biodiversity of Antarctic and Sub-Antarctic Ecosystems, Santiago, Chile
  • Manuel Dall’Osto Department of Marine Biology and Oceanography, Institute of Marine Sciences, Barcelona, Spain
  • Fabio L.V. Bones Pós Graduação em Fungos, Algas e Plantas, Universidade Federal de Santa Catarina, Florianopolis, Brazil
  • Micheline Carvalho-Silva Departamento de Botânica, Universidade de Brasília, Brasília, Brazil
  • Diego Knop Henriques Departamento de Botânica, Universidade de Brasília, Brasília, Brazil
  • Luiz Henrique Rosa Departamento de Microbiologia, Universidade Federal de Minas Gerais, Brazil
Keywords: High throughput sequencing, dispersal, Algae, Plants, Protozoa, Animalia

Abstract

A major natural route of dispersal to Antarctica is often assumed to be atmospheric transport, although few studies have documented this in detail. Aerial dispersal to Antarctica is very challenging as the continent is geographically remote from other land areas and is isolated by the atmospheric circumpolar vortex. Detailed information about aerial routes by which microorganisms arrive and circulate in Antarctica is generally lacking, as few aerobiological studies have focused on eukaryotes and those that have predominantly relied on traditional morphological identification. Recent advances in molecular biology, such as DNA metabarcoding by high throughput sequencing (HTS), have provided a powerful new tool for the study of atmospheric biological diversity and can retrieve levels of diversity an order of magnitude higher than traditional methods. In this study, we used HTS to investigate the diversity of non-fungal eukaryotes present in the atmosphere and freshly precipitated snow on Livingston Island. In a total of 740 m3 of air and 3.76 L of snow sampled, representatives of four kingdoms (Protozoa, Chromista, Viridiplantae and Animalia) and five phyla (Ciliophora, Ochrophyta, Chlorophyta, Magnoliophyta and Porifera) were found. The most diverse phylum was Chlorophyta, represented in our samples by 10 taxa, with Trebouxia asymmetrica Friedl & Gärtner the most abundant representative.

Downloads

Download data is not yet available.

References


Abarenkov K., Zirk A., Piirmann T., Pöhönen R., Ivanov F., Nilsson R.H. & Kõljalg U. 2020. UNITE QIIME release for fungi. Version 04.02.2020. (Data set.) UNITE Community. doi: 10.15156/BIO/786385.




Adl S.M., Bass D, Lane C.E., Lukeš J., Schoch C.L., Smirnov A., Agatha S., Berney C., Brown M.W., Burki F., Cárdenas P., CˇepiCˇka I., Chistyakova L., Del Campo J., Dunthorn M., Edvardsen B., Eglit Y., Guillou L., Hampl V., Heiss A.A., Hoppenrath M., James T.Y., Karnkowska A., Karpov S., Kim E., Kolisko M., Kudryavtsev A., Lahr D.J.G., Lara E., Le Gall L., Lynn H., Mann D.G., Massana R., Mitchell E.A.D., Morrow C., Park J.S., Pawlowski J.W., Powell M.J., Richter D.J., Rueckert S., Shadwick L., Shimano S., Spiegel F.W., Torruella G., Youssef N., Zlatogursky V. & Zhang Q. 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. Journal of Eukaryotic Microbilogy 66, 4–119, doi: 10.1111/jeu.12691.




Archer S.D.J., Lee K.C., Caruso T., Maki T., Lee C.K., Cary S.C., Cowan D.A., Maestre F.T. & Pointing S. 2019. Airborne microbial transport limitation to isolated Antarctic soil habitats. Nature Microbiology 4, 925–932, doi: 10.1038/s41564-019-0370-4.




Banchi E., Ametrano C.G., Greco S., Stanković D., Muggia L. & Pallavicini A. 2020. PLANiTS: a curated sequence reference dataset for plant ITS DNA metabarcoding. Database 2020, baz155, doi: 10.1093/database/baz155.




Bardou P., Mariette J., Escudié F., Djemiel C. & Klopp C. 2014. Jvenn: an interactive Venn diagram viewer. BMC Bioinformatics 15, article no. 293, doi: 10.1186/1471-2105-15-293.




Bokulich N.A., Kaehler B.D., Rideout J.R., Dillon M., Boylern E., Knight R., Huttley G.A. & Caporaso J.G. 2018. Optimizing taxonomic classification of marker‐gene amplicon sequences with QIIME 2’s q2‐feature‐classifier plugin. Microbiome 6, 90–107, doi: 10.1186/s40168-018-0470-z.




Bottos E.M., Woo A.C., Zawar-Reza P., Pointing S.B. & Cary S.C. 2013. Airborne bacterial populations above desert soils of the McMurdo Dry Valleys, Antarctica. Microbial Ecology 67, 120–128, doi: 10.1007/s00248-013-0296-y.




Bracegirdle T.J., Krinner G., Tonelli M., Haumann F.A., Naughten K.A., Rackow T., Roach L.A. & Wainer I. 2020. Twenty first century changes in Antarctic and Southern Ocean surface climate in CMIP6. Atmospheric Science Letters 21, e984, doi: 10.1002/asl.984.




Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K. & Madden T.L. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10, article no. 421, doi: 10.1186/1471-2105-10-421.




Câmara P.E.A.S., Carvalho-Silva M., Pinto O.H.B., Amorim E.T., Henriques D.K., Silva T.H., Pellizzari F., Convey P. & Rosa L.H. 2021. Diversity and ecology of Chlorophyta (Viridiplantae) assemblages in protected and non-protected sites in Deception Island (Antarctica, South Shetland Islands) assessed using an NGS approach. Microbial Ecology 81, 323–334, doi: 10.1007/s00248-020-01584-9.




Câmara P.E.A.S., Convey P., Rangel S.B., Konrath M., Barreto C.C., Pinto O.H.B., Carvalho-Silva M., Henriques D.K., Oliveira H.C. & Rosa L.H. 2021. The largest moss carpet transplant in Antarctica and its bryosphere cryptic biodiversity. Extremophiles 25, 369–384, doi: 10.1007/s00792-021-01235-y.




Câmara P.E.A.S., de Menezes G.C.A., Oliveira F.S., Delpuppo C., Schaefer C.E.G.R, Convey P., Pinto O.H.B., Carvalho-Silva M. & Rosa L.H. 2022. Diversity of Viridiplantae DNA present on rock surfaces in the Ellsworth Mountains, continental Antarctica. Polar Biology 45, 637–646, doi: 10.1007/s00300-022-03021-8.




Campos M., Mothes B. & Mendes I.L.V. 2007. Antarctic sponges (Porifera, Demospongiae) of the South Shetland Islands and vicinity: part II. Poecilosclerida. Revista Brasileira de Zoologia 24, 742–770, doi: 10.1590/S0101-81752007000300027.




Carvalho-Silva M., Rosa L.H., Pinto O.H.B., Da Silva T., Henriques D.K., Convey P. & Câmara P.E.A.S. 2021. Exploring the plant environmental DNA diversity in soil from two sites on Deception Island (Antarctica, South Shetland Islands) using metabarcoding. Antarctic Science 33, 469–478, doi: 10.1017/S0954102021000274.




Chen S., Yao H., Han J., Liu C., Song J., Shi L., Zhu Y., Ma X., Gao T., Pang X., Luo K., Li W., Li X, Jia X, Lin Y. & Leon C. 2010. Validation of the ITS2 region as a novel DNA barcode for identifying medicinal plant species. PLoS One 5, e8613, doi: 10.1371/journal.pone.0008613.




Convey P. & Peck L.S. 2019. Antarctic environmental change and biological responses. Science Advances 5, eaaz0888, doi: 10.1126/sciadv.aaz0888.




Czechowski P., Clarke L., Cooper A. & Stevens M. 2017. A primer to metabarcoding surveys of Antarctic terrestrial biodiversity. Antarctic Science 29, 3–15, doi: 10.1017/S0954102016000389.




Deiner K., Bik H.M., Mächler E., Seymour M., Lacoursière-Roussel A., Altermatt F., Creer S., Bista I., Lodge DM, de Vere N., Pfrende M.E. & Bernatchez L. 2017. Environmental DNA metabarcoding: transforming how we survey animal and plant communities. Molecular Ecology 26, 5872–5895, doi: 10.1111/mec.14350.




Hammer Ø., Harper D.A.T. & Ryan P.D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, article no. 4.




Headland R. 2009. A chronology of Antarctic exploration: a synopsis of events and activities from the earliest times until the International Polar Years, 2007–09. London: Bernard Quaritch.




Hering D., Borja A., Jones J.I., Pont D., Boets P., Bouchez A., Bruce K., Drakare S., Hanfling B., Kahlert M., Leese F., Meissner K., Mergen P., Reyjol Y., Segurado P., Vogler A. & Kelly M. 2018. Implementation options for DNA-based identification into ecological status assessment under the European Water Framework Directive. Water Research 138, 192–205, doi: 10.1016/j.watres.2018.03.003.




Hughes K.A., McCartney H.A., Lachlan-Cope T.A. & Pearce D.A. 2004. A preliminary study of airborne microbial biodiversity over peninsular Antarctica. Cellular and Molecular Biology 50, 537–42.




Ivanov L. 2009. Antarctica: Livingston Island and Greenwich, Robert, Snow and Smith islands. Scale 1:120000 topographic map. Troyan, Bulgaria: Manfred Wörner Foundation.




Lee J., Do Hur S., Lim H.S. & Jung H. 2020. Isotopic characteristics of snow and its meltwater over the Barton Peninsula, Antarctica. Cold Regions Science and Technology 173, article no. 102997, doi: 10.1016/j.coldregions.2020.102997.




Marshall W.A. 1996. Aerial dispersal of lichen soredia in the maritime Antarctic. New Phytologist 134, 523–30, doi: 10.1111/j.1469-8137.1996.tb04370.x.




Marshall W.A. & Chalmers M.O. 1997. Airborne dispersal of Antarctic terrestrial algae and cyanobacteria. Ecography 20, 585–94, doi: 10.1111/j.1600-0587.1997.tb00427.x.




Marshall W.A. & Convey P. 1997. Dispersal of moss propagules on Signy Island, maritime Antarctic. Polar Biology 18, 376–383, doi: 10.1007/s003000050203




Pearce D.A., Alekhina I.A., Terauds A., Wilmotte A., Quesada A., Edwards A., Dommergue A., Sattler B., Adams B.J., Magalhães C., Chu W.L., Lau M.C.Y., Cary C., Smith D.J., Wall D., Euguren G., Matcher G., Bradley J.A., De Vega P., Elster J., Hughes K.A., Cuthbertson L., Benning L.G., Gunde-Cimerman N., Convey P., Hong S.G., Pointing S.B., Pellizari V.H. & Vincent W.F. 2016. Aerobiology over Antarctica—a new initiative for atmospheric ecology. Frontiers in Microbiology 16, 7–16, doi: 10.3389/fmicb.2016.00016.




Pearce D.A., Hughes K.A., Lachlan-Cope T., Harangozo S.A. & Jones A.E. 2010. Biodiversity of airborne microorganisms at Halley Station, Antarctica. Extremophiles 14, 145–159, doi: 10.1007/s00792-009-0293-8.




Richardson R.T., Lin C., Sponsler D.B., Quijia J.O., Goodell K. & Johnson R.M. 2015. Application of ITS2 metabarcoding to determine the provenance of pollen collected by honey bees in an agroecosystem. Applications in Plant Sciences 3, article no. 1400066, doi: 10.3732/apps.1400066.




Rippin M., Borchhardt N., Williams L., Colesie C., Jung P., Büdel B., Karsten U. & Becker B. 2018. Genus richness of microalgae and cyanobacteria in biological soil crusts from Svalbard and Livingston Island: morphological versus molecular approaches. Polar Biology 41, 909–923, doi: 10.1007/s00300-018-2252-2.




Rosa L.H., Pinto O.H.B., Convey P., Carvalho-Silva M., Rosa C.A. & Câmara P.E.A.S. 2021. DNA metabarcoding to assess the diversity of airborne fungi present over Keller Peninsula, King George Island, Antarctica. Microbial Ecology 82, 165–172, doi: 10.1007/s00248-020-01627-1.




Rosa L.H., Pinto O.H.B., Šantl-Temkiv T., Convey P., Carvalho-Silva M., Rosa C.A. & Rosa L.H. 2020. DNA metabarcoding of fungal diversity in air and snow of Livingston Island, South Shetland Islands, Antarctica. Scientific Reports 10, article no. 21793, doi: 10.1038/s41598-020-78630-6.




Ruggiero M.A., Gordon D.P., Orrell T.M., Bailly N., Bourgoin T., Brusca R.C., Cavalier-Smith T., Guiry M.D. & Kirk P.M. 2015. Correction: a higher-level classification of all living organisms. PLoS One 10(6), e0130114, doi:10.1371/journal.pone.0130114.




Ruppert K., Kline R.J. & Rahman M.S. 2019. Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: a systematic review in methods, monitoring, and applications of global eDNA. Global Ecology and Conservation 17, e00547, doi: 10.1016/j.gecco.2019.e00547.




Šantl-Temkiv T., Amato P., Gosewinkel U., Thyrhaug R., Charton A., Chicot B., Bratbak G. & Löndahl. 2017. High-flow-rate impinger for the study of concentration, viability, metabolic activity, and ice-nucleation activity of airborne bacteria. Environmental Science and Technology 51, 11224–11234, doi: 10.1021/acs.est.7b01480.




Šantl-Temkiv T., Gosewinkel U., Starnawski P., Lever M. & Finster K. 2018. Aeolian dispersal of bacteria in southwest Greenland: their sources, abundance, diversity and physiological states. FEMS Microbiology Ecology 94, fiy031, doi: 10.1093/femsec/fiy031.




Šantl-Temkiv T., Sikoparija B., Maki T., Carotenuto F., Amato P., Yao M., Morris C.E., Schnell R., Jaenicke R., Pöhlker C., DeMott P.J. Hill T.C.J. & Huffman J.A. 2020. Bioaerosol field measurements: challenges and perspectives in outdoor studies. Aerosol Science and Technology 54, 520–546, doi: 10.1080/02786826.2019.1676395.




Seckbach J. 2002. Symbiosis: mechanisms and model systems. Dordrecht: Kluwer Academic.




Siegert M.J., Barret P., DeConto R., Dunbar R., Cofaigh C., Passchier S. & Naish T. 2008. Recent advances in understanding Antarctic climate evolution. Antarctic Science 20, 313–325, doi:10.1017/S0954102008000941.




Sundberg S. 2013. Spore rain in relation to regional sources and beyond. Ecography 36, 364–373, doi: 10.1111/j.1600-0587.2012.07664.x.




Tesson S.V.M. & Šantl-Temkiv T. 2018. Ice nucleation activity and aeolian dispersal success in airborne and aquatic microalgae. Frontiers in Microbiology 9, article no. 2681, doi: 10.3389/fmicb.2018.02681.




Turner J., Bindschadler R., Convey P., di Prisco G., Fahrbach E., Gutt J., Hodgson D., Mayewski P. & Summerhayes C. (eds.) 2009. Antarctic climate change and the environment. Cambridge: Scientific Committee on Antarctic Research.




Turner J., Lu H., White I., Phillips T., Hosking J.S., Bracegirdle T.J., Marshall G., Mulvaney R. & Deb P. 2016. Absence of 21st century warming on Antarctic Peninsula consistent with natural variability. Nature 535, 411–415, doi: 10.1038/nature18645.




White T.J., Bruns T., Lee S. & Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M.A. Innis et al. (eds.): PCR protocols: a guide to methods and applications. Pp. 315–322. London: Academic Press.
Published
2025-03-14
How to Cite
Câmara , P. E., Šantl‑Temkiv , T., Pinto , O. H., Convey , P., Dall’Osto , M., Bones , F. L., Carvalho-Silva , M., Henriques , D. K., & Rosa , L. H. (2025). DNA metabarcoding of non-fungal eukaryotic diversity in air and snow of Livingston Island, South Shetland Islands, Antarctica. Polar Research, 44. https://doi.org/10.33265/polar.v44.8293
Section
Research Articles