Abstract
Snow is a unique microhabitat, despite being a harsh environment, multiple life forms have adapted to survive in it. While algae, bacteria and fungi are dominant microorganisms in Antarctic snow, little is known about other organisms that may be present in this habitat. We used metabarcoding to investigate DNA sequence diversity of non-fungal eukaryotes present in snow obtained from six different sites across the Maritime Antarctica. A total of 20 taxa were assigned to obtained sequences, representing five Kingdoms (Chromista, Protozoa, Viridiplantae and Metazoa) and four phyla (Ciliophora, Cercozoa, Chlorophyta and Cnidaria). The highest diversity indices were detected in Trinity Peninsula followed by Robert Island, Arctowski Peninsula, Deception Island, King George Island and Snow Island. The most abundant assignments were to Trebouxiophyceae, followed by Chlamydomonas nivalis and Chlamidomonadales. No taxa were detected at all sites. Three potentially new records for Antarctica were detected: two Ciliophora (Aspidisca magna and Stokesia sp.) and the green algae Trebouxia potteri. Our data suggested that similarities found between the sites may be more related with snow physicochemical properties rather than geographic proximity or latitude. This study provides new insights into the diversity and distribution of eukaryotic organisms in Antarctic snow.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abarenkov K, Zirk A, Piirmann T, Pöhönen R, Ivanov F., Nilsson RH, Kõljalg U (2020) UNITE QIIME release for Fungi. Version 04.02.2020. UNITE Community. https://doi.org/10.15156/BIO/786385
Banchi E, Ametrano CG, Greco S, Stanković D, Muggia L, Pallavicini A (2020) PLANiTS: a curated sequence reference dataset for plant ITS DNA metabarcoding. Database 2020:baz155. https://doi.org/10.1093/database/baz155
Bardou P, Mariette J, Escudié F, Djemiel C, Klopp C (2014) Jvenn: an interactive Venn diagram viewer. BMC Bioinformatics 15:1–7. https://doi.org/10.1186/1471-2105-15-293
Berger H (1999) Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monographiae Biologicae, vol 78. Springer, Dordrecht
Berger H (2008) Monograph of the Amphisiellidae and Trachelostylidae (Ciliophora, Hypotricha). Monographiae Biologicae, vol 88. Springer, Dordrecht
Berger H (2011) Monograph of the Gonostomatidae and Kahliellidae (Ciliophora, Hypotricha). Monographiae Biologicae, vol 90. Springer, Dordrecht
Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Boylern E, Knight R, Huttley GA, Caporaso JG (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6:90–107. https://doi.org/10.1186/s40168-018-0470-z
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, AlGhalith A, Alexander H, Alm EJ, Arumugan M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Chase J, Cope EK, Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzales A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu Y, Loftfield LC, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, NavasMolina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS II, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasa S, van der Hoof JJJ, Vargas F, Vazques-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (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
Bracegirdle TJ, Krinner G, Tonelli M, Haumann FA, Naughten KA, Rackow T, Roach LA, Wainer I (2020) Twenty first century changes in Antarctic and Southern Ocean surface climate in CMIP6. Atmos Sci Lett. https://doi.org/10.1002/asl.984
Bushnell B (2014) BBMap: a fast, accurate, splice-aware aligner. Lawrence Berkeley National Lab (LBNL), Berkeley
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
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10(1):1–9. https://doi.org/10.1186/1471-2105-10-421
Câmara PEAS, Carvalho-Silva M, Pinto OHB, Amorim ET, Henriques DK, Silva TH, Pellizzari F, Convey P, Rosa LH (2021a) Diversity and ecology of chlorophyta (Viridiplantae) assemblages in protected and non-protected sites in deception island (Antarctica. Microb Ecol, South Shetland Islands) assessed using an NGS approach. Microb Ecol 81:323–334. https://doi.org/10.1007/s00248-020-01584-9
Câmara PEAS, Convey P, Rangel SB, Konrath M, Barreto CC, Pinto OHB, Carvalho-Silva M, Henriques DK, Oliveira HC, Rosa LH (2021b) The largest moss carpet transplant in Antarctica and its bryosphere cryptic biodiversity. Extremophiles 25:369–384. https://doi.org/10.1007/s00792-021-01235-y
Câmara PEAS, de Menezes GCA, Oliveira FS, Souza CD, Amorim ET, Schaefer CEGR, Convey P, Pinto OHB, Carvalho-Silva M, Rosa LH (2022) Diversity of Viridiplantae DNA present on rock surfaces in the Ellsworth Mountains, continental Antarctica. Polar Biol 45:637–646. https://doi.org/10.1007/s00300-022-03021-8
Carvalho-Silva M, Rosa L, Pinto OHB, Da Silva T, Henriques D, Convey P, Câmara PEAS (2021) Exploring the plant environmental DNA diversity in soil from two sites on Deception Island (Antarctica, South Shetland Islands) using metabarcoding. Antarct Sci. https://doi.org/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 Y, 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. https://doi.org/10.1371/journal.pone.0008613
Davey MP, Norman L, Sterk P, Huete-Ortega M, Bunbury F, Loh BKW, Stockton S, Peck LS, Convey P, Newsham K, Smith AG (2019) Snow algae communities in Antarctica—metabolic and taxonomic composition. New Phytol 222:1242–1255. https://doi.org/10.1111/nph.15701
de Menezes GCA, Amorim SS, Gonçalves VN, Godinho VM, Simões JC, Rosa CA, Rosa LH (2019) Diversity, distribution, and ecology of fungi in the seasonal snow of Antarctica. Microorganisms 7:445. https://doi.org/10.3390/microorganisms7100445
de Menezes GCA, Câmara PEAS, Pinto OHB, Convey P, Carvalho-Silva M, Simões JC, Rosa CA, Rosa LH (2022) 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. https://doi.org/10.1007/s00248-021-01792-x
Deiner K, Bik HM, Mächler E, Seymour M, Lacoursière-Roussel A, Altermatt F, Creer S, Bista I, Lodge DM, de Vere N, Pfrender ME, Bernatchez L (2017) Environmental DNA metabarcoding: transforming how we survey animal and plant communities. Mol Ecol 26:5872–5895. https://doi.org/10.1111/mec.14350
Delphy J (1938) Les Actinies Athénaires (Actiniaria Abasiliaria) de la Faune Française. Bull Mus Hist Nat Paris 2:619–622
Esteban GF, Finlay BJ (2007) Exceptional species richness of ciliated protozoa in pristine intertidal rock pools. Mar Ecol Prog Ser 335:133–214. https://doi.org/10.3354/meps335133
Foissner W (1998) An updated compilation of world soil ciliates (Protozoa, Ciliophora), with ecological notes, new records, and descriptions of new species. Eur J Protistol 34:195–235. https://doi.org/10.1016/S0932-4739(98)80028-X
Foissner W (2014) An update of ‘basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa. Int J Syst Evol Microb 64:271–292. https://doi.org/10.1099/ijs.0.057893-0
Gotelli NJ, Ellison AM (2004) A primer of ecological statistics, vol 1. Sinauer Associates, Sunderland
Guiry MD, Guiry GM (2023) AlgaeBase. World-wide electronic publication. https://www.algaebase.org
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Pal Elec 4:1–9
Hering D, Borja A, Jones JI, 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 Res 138:192–205. https://doi.org/10.1016/j.watres.2018.03.003
Hudson DH, Beier S, Flade I, Górska A, El-Hadidi M, Mitra S et al (2016) MEGAN community editioninteractive exploration and analysis of large-scale microbiome sequencing data. PLoS Comp Biol 12(6):e1004957. https://doi.org/10.1371/journal.pcbi.1004957
Huss V, Frank C, Hartmann EC, Hirmer M (1999) Biochemical taxonomy and molecular phylogeny of the genus Chlorella sensu lato (Chlorophyta). J Phycol 35(3):587–598. https://doi.org/10.1046/j.1529-8817.1999.3530587.x
Kahl A (1932) Urtiere oder Protozoa. Tierwelt Deutschl 25:399–650
Kloser, H. (1990) Distribution of microplankton organisms north and west of the Antarctic Peninsula according to changing ecological conditions in autumn. Berichte zur Polarforschung 77:1–255
Küppers GC, Paiva TdaS, Borges BdoN, Harada ML, Garraza GG, Mataloni G (2011) An Antarctic hypotrichous ciliate, Parasterkiella thompsoni (Foissner) nov. gen., nov. comb., recorded in Argentinean peat-bogs: morphology, morphogenesis, and molecular phylogeny. Eur J Protistol 47:103–123. https://doi.org/10.1016/j.ejop.2011.01.002
Legendre P, Legendre L (2012) Numerical ecology. Elsevier, Amsterdam
Li L, Song W, Al-Rasheid KAS, Warren A, Li Z, Xu W, Shao C (2010) Morphology and morphogenesis of a new marine hypotrichous ciliate (Protozoa, Ciliophora, Pseudoamphisiellidae), including a report on the small subunit rRNA gene sequence. Zool J Linn Soc 158:231–243. https://doi.org/10.1111/j.1096-3642.2009.00546.x
Li T, Liu M, Warren A, Al-Farraj SA, Yi Z, Sheng Y (2022) Morphology and SSU rRNA gene-based phylogeny of three peniculid ciliates (Ciliophora, Oligohymenophorea) from China, including a new Frontonia species. Eur J Prot 85:125910. https://doi.org/10.1016/j.ejop.2022.125910
Lopatina A, Krylenkov V, Severinov K (2013) Activity and bacterial diversity of snow around Russian Antarctic stations. Res Microbiol 164:949–958. https://doi.org/10.1016/j.resmic.2013.08.005
Lynn DH (2008) The Ciliated Protozoa: characterization, classification, and guide to the literature, 3rd edn. Springer, Dordrecht
Magurran AE (2021) Measuring biological diversity. Current Biol 31:R1174–R1177. https://doi.org/10.1016/j.cub.2021.07.049
Margesin R, Miteva V (2011) Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162:346–361. https://doi.org/10.1016/j.resmic.2010.12.004
Paiva TS (2020) Systematic redefinition of the hypotricha (alveolata, ciliophora) based on combined analyses of morphological and molecular characters. Protist 171(4):125755. https://doi.org/10.1016/j.protis.2020.125755
Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87(10):2614–2625. https://doi.org/10.1890/0012-9658(2006)87[2614:VPOSDM]2.0.CO;2
Petz W, Foissner W (1997) Morphology and infraciliature of some soil ciliates (Protozoa, Ciliophora) from continental Antarctica, with notes on the morphogenesis of Sterkiella histriomuscorum. Polar Rec 33:307–326. https://doi.org/10.1017/S0032247400025407
Petz W, Song W, Wilbert N (1995) Taxonomy and ecology of theciliate fauna (Protozoa, Ciliophora) in the endopagial and pelagial of the Weddell Sea, Antarctica. Stapfia 40:1–223
Richardson RT, Lin C, Sponsler DB, Quijia JO, Goodell K, Johnson RM (2015) Application of ITS2 metabarcoding to determine the provenance of pollen collected by honey bees in an agroecosystem. Appl Plant Sci 3:1400066. https://doi.org/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 Biol 41:909–923. https://doi.org/10.1007/s00300-018-2252-2
Rosa LH, Pinto OHB, Šantl-Temkiv T, Convey P, Carvalho-Silva M, Rosa CA, Câmara PEAS (2020) DNA metabarcoding of fungal diversity in air and snow of Livingston Island, South Shetland Islands, Antarctica. Sci Rep 10:21793. https://doi.org/10.1038/s41598-020-78630-6
Ruppert K, Kline RJ, Rahman MS (2019) Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: a systematic review in methods, monitoring, and applications of global eDNA. Glob Ecol Cons 17:e00547. https://doi.org/10.1016/j.gecco.2019.e00547
Šantl-Temkiv T, Amato P, Casamayor EO, Lee PKH, Pointing SB (2022) Microbial ecology of the atmosphere. FEMS Microb Rev 46(4):fuac009. https://doi.org/10.1093/femsre/fuac009
Siegert M, Bentley M, Atkinson A, Bracegirdle T, Convey P, Davies B, Downie R, Hogg AE, Holmes C, Hughes K, Meredith M, Ross N, Rumble J, Wilkinson J (2023) Antarctic Extreme Events. Front Environ Sci 11:1229283. https://doi.org/10.3389/fenvs.2023.1229283
Song W, Wilbert N (2000) Ciliates from Antarctic sea ice. Polar Biol 23:212–222. https://doi.org/10.1007/s003000050029
Song W, Wilbert N (2002) Faunistic studies on marine ciliates from the Antarctic benthic area, including descriptions of one epizoic form, 6 new species and 2 new genera (Protozoa: Ciliophora). Acta Protozool 41:23–61
Soto DF, Fuentes R, Huovinen P, Gómez I (2020) Microbial composition and photosynthesis in Antarctic snow algae communities: Integrating metabarcoding and pulse amplitude modulation fluorometry. Algal Res 45:101738. https://doi.org/10.1016/j.algal.2019.101738
Taş N, Jong AEE, Li Y, Trubl G, Xue Y, Dove NC (2021) Metagenomic tools in microbial ecology research. Curr Opin Biotechnol 67:184–191. https://doi.org/10.1016/j.copbio.2021.01.019
Thompson A, Powell G, Adams B (2019) Provisional checklist of terrestrial heterotrophic protists from Antarctica. Ant Sci 31(6):287–303. https://doi.org/10.1017/S0954102019000361
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. Scientific Committee on Antarctic Research, Cambridge
Turner J, Lu H, White I, Phillips T, Hosking JS, Bracegirdle TJ, Marshall G, Mulvaney R, Deb P (2016) Absence of 21st century warming on Antarctic Peninsula consistent with natural variability. Nature 535:411–415. https://doi.org/10.1038/nature18645
Vacelet E (1961) La faune infusorienne des “sables a amphioxus” des environs de Marseille. Bull Inst Oceanogr Monaco 58(1202):1–12
Valbonesi A (1996) Description of a new species of Aspidisca, Aspidisca terranovae sp. n., from Antarctica (Ciliophora, Hypotrichida). Ital J Zool 63:377–380. https://doi.org/10.1080/11250009609356162
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. Academic Press, London, pp 315–322
Williams RB (1981) A sea anemone, Edwardsia meridionalis sp. nov., from Antarctica and a preliminary revision of the genus Edwardsia de Quatrefages, 1841 (Coelenterata: Actiniaria). Rec Aust Mus 336:325–360. https://doi.org/10.3853/j.0067-1975.33.1981.271
Acknowledgements
This study received financial support from Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Ministério da Ciência, Tecnologia e Inovação (MCTI), Programa Antártico Brasileiro (PROANTAR), CAPES and FAPEMIG. We thank the crews of the polar vessels Ary Rongel and Alte Maximiano. P. Convey is supported by Natural Environment Research Council (NERC) core funding to the British Antarctic Survey’s (BAS) ‘Biodiversity, Evolution and Adaptation’ Team. Thanks also to congresswoman Jô Moraes, to the Instituto de Ciências Biológicas at Universidade de Brasília and to the Brazilian Navy and Air Force for logistic support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Oren.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Câmara, P.E.A.S., de Menezes, G.C.A., Lopes, F.A.C. et al. Investigating non-fungal eukaryotic diversity in snow in the Antarctic Peninsula region using DNA metabarcoding. Extremophiles 28, 3 (2024). https://doi.org/10.1007/s00792-023-01322-2
Received:
Accepted:
Published:
Version of record:
DOI: https://doi.org/10.1007/s00792-023-01322-2