Skip to main content

Advertisement

Log in

Phylogenetic diversity and dominant ecological traits of freshwater Antarctic Chrysophyceae

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Previous studies conducted in summer in the lakes at Hope Bay (Antarctic Peninsula) between 1991 and 2007 showed a large numerical contribution of flagellated Chrysophyceae to the phytoplankton communities, particularly in the oligotrophic lakes, as evidenced by light microscopy observations and molecular fingerprinting. Given the ecological relevance of this group in these Antarctic microbial foodwebs, we carried out further molecular analyses (clone libraries and 18S Illumina high throughput sequencing) to characterize their phylogenetic diversity. The results of this study significantly increased the retrieved Chrysophyceae biodiversity. Clone libraries in two selected lakes (one oligotrophic and one mesotrophic) yielded 12 different chrysophycean OTUs, whereas 81 Swarm OTUs were recovered from six lakes using Illumina HiSeq. With the combination of both methods, we observed sequences of all the chrysophyte known clades, although most of the diversity belonged to Clade D, a group comprising mixotrophic and heterotrophic species. The percentage of reads for this clade in Illumina HiSeq ranged from 30% to 96% of the total Chrysophyceae reads. Based on experiments and observations, we also describe the main ecological traits of this group: the dominant taxa were small pigmented flagellates, well adapted to survive in oligotrophic systems, sometimes abundant under ice-cover subjected to low light intensities, and that have phagotrophic behavior. The used combination of methods allowed us to characterize the biodiversity and ecology of the Chrysophyceae, the dominant phytoplankton group in the oligotrophic lakes of this Maritime Antarctic region.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM (2009) A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS One 4:10–1371

    Article  PubMed Central  Google Scholar 

  • Allende L, Izaguirre I (2003) The role of the physical stability on the establishment of steady states in the phytoplankton community of two maritime Antarctic lakes. Hydrobiologia 502:211–224

    Article  Google Scholar 

  • Allende L, Pizarro H (2006) Top-down control on plankton components in an Antarctic pond: experimental approach to the study of low-complexity food webs. Polar Biol 29(10):893–901

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersen RA (2007) Molecular Systematics of the Chrysophyceae and Synurophyceae. In: Brodie J, Lewis J (eds): Unravelling the algae: The past, present and future of algal systematics, Taylor and Francis, USA

  • Bell EM, Laybourn-Parry J (2003) Mixotrophy in the Antarctic phytoflagellate, Pyramimonas gelidicola (Chlorophyta: Prasinophyceae). J Phycol 39:644–649

    Article  Google Scholar 

  • Berger SA, Krompass D, Stamatakis A (2011) Performance, accuracy, and web server for evolutionary placement of short sequence reads under maximum likelihood. Syst Biol 60:291–302

    Article  PubMed  PubMed Central  Google Scholar 

  • Bird DF, Kalff J (1986) Bacterial grazing by planktonic lake algae. Science 231(4737):493–495

    Article  CAS  PubMed  Google Scholar 

  • Bird DF, Kalff J (1987) Algal phagotrophy: Regulating factors and importance relative to photosynthesis in Dinobryon (Chrysophyseae). Limnol Oceanogr 32:277–284

    Article  CAS  Google Scholar 

  • Bird DF, Kalff J (1989) Phagotrophic sustenance of a metalimnetic phytoplankton peak. Limnol Oceanogr 34:155–162

    Article  Google Scholar 

  • Boenigk J, Pfandl K, Stadler P, Chatzinotas A (2005) High diversity of the ‘Spumella-like’ flagellates: an investigation based on the SSU rRNA gene sequences of isolates from habitats located in six different geographic regions. Environ Microbiol 7:685–697

    Article  CAS  PubMed  Google Scholar 

  • Butler HG (1999) Seasonal dynamics of the planktonic microbial community in a maritime Antarctic lake undergoing eutrophication. J Plankton Res 21:2393–2419

    Article  Google Scholar 

  • Cavalier-Smith T, Chao EE (2006) Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). J Mol Evol 62:388–420

    Article  CAS  PubMed  Google Scholar 

  • Charvet S, Vincent WF, Lovejoy C (2012) Chrysophytes and other protists in High Arctic lakes: molecular gene surveys, pigment signatures and microscopy. Polar Biol 35:733–748

    Article  Google Scholar 

  • Debroas D, Hugoni M, Domaizon I (2015) Evidence for an active rare biosphere within freshwater protists community. Mol Ecol 24:1236–1247

    Article  CAS  PubMed  Google Scholar 

  • Debroas D, Domaizon I, Humbert J-F, Jardillier L, Lepère C, Oudart A, Taïb N (2017) Overview of freshwater microbial eukaryotes diversity: a first analysis of publicly available metabarcoding data. FEMS Microbiol Ecol 93(4):1. https://doi.org/10.1093/femsec/fix023

    Article  CAS  Google Scholar 

  • del Campo J, Massana R (2011) Emerging diversity within chrysophytes, choanoflagellates and bicosoecids based on molecular surveys. Protist 162:435–448

    Article  PubMed  Google Scholar 

  • de Vargas C, Audic S, Henry N, Decelle J, Mahe F, Logares R et al (2015) Eukaryotic plankton diversity in the sunlit ocean. Science 348:1261605

    Article  PubMed  Google Scholar 

  • Díez B, Pedros-Alió C, Massana R (2001) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl Environ Microbiol 67:2932–2941

    Article  PubMed  PubMed Central  Google Scholar 

  • Domaizon I, Viboud S, Fontvieille D (2003) Taxon-specific and seasonal variations in flagellates grazing on heterotrophic bacteria in the oligotrophic Lake Annecy–importance of mixotrophy. FEMS Microbiol Ecol 46(3):317–329

    Article  CAS  PubMed  Google Scholar 

  • Drago E, Paira A (1987) Informe de la campaña antártica de verano 1986/87. Instituto Antártico Argentino, Buenos Aires

    Google Scholar 

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

    Article  Google Scholar 

  • Elwood HJ, Olsen GJ, Sogin ML (1985) The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Mol Biol Evol 2:399–410

    CAS  PubMed  Google Scholar 

  • Epstein SS, Shiaris MP (1992) Size-selective grazing of coastal bacterioplankton by natural assemblages of pigmented flagellates, colorless flagellates, and ciliates. Microbial Ecol 23(3):211–225

    Article  CAS  Google Scholar 

  • Epstein S, López-García P (2008) ‘“Missing”’ protists: a molecular prospective. Biodivers Conserv 17:261–276

    Article  Google Scholar 

  • Ernst A, Becker S, Wollenzien VIA, Postius C (2003) Ecosystem dependent adaptive radiations of Picocyanobacteria inferred from 16S rRNA and ITS-1 sequence analysis. Microbiology 149:217–228

    Article  CAS  PubMed  Google Scholar 

  • Ettl H (1983) Chlorophyta I. Phytomonadina. In: Ettl H, Gerloff J, Heynig H, Mollenhauer D (eds) SüBwasserflora von Mitteleuropa, 9, Gustav Fischer, Stuttgart

  • Gerea M, Queimaliños C, Schiaffino MR, Izaguirre I, Forn I, Massana R, Unrein F (2013) In situ prey selection of mixotrophic and heterotrophic flagellates in Antarctic oligotrophic lakes: an analysis of the digestive vacuole content. J Plankton Res 35(1):201–212

    Article  Google Scholar 

  • Gerea M, Saad JF, Izaguirre I, Queimaliños C, Gasol JM, Unrein F (2016) Presence, abundance and bacterivory of the mixotrophic algae Pseudopedinella (Dictyochophyceae) in freshwater environments. Aquat Microb Ecol 76:219–232

    Article  Google Scholar 

  • Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L et al (2013) The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy. Nucleic Acids Res 41:D597–D604

    Article  CAS  PubMed  Google Scholar 

  • Graupner N, Jensen M, Bock C, Marks S, Rahmann S, Beisser D, Boenigk J (2018) Evolution of heterotrophy in chrysophytes as reflected by comparative transcriptomics. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiy039

    Article  PubMed  PubMed Central  Google Scholar 

  • Grossmann L, Bock C, Schweikert M, Boenigk J (2016) Small but manifold – hidden diversity in “Spumella-like Flagellates.” J of Eukaryot Microbiol 63:419–439

    Article  Google Scholar 

  • Havskum H, Riemann B (1996) Ecological importance of bacterivorous, pigmented flagellates (mixotrophs) in the Bay of Aarhus, Denmark. Mar Ecol Prog Ser 137:251–263

    Article  Google Scholar 

  • Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424

    Article  Google Scholar 

  • Hitchman RB, Jones HL (2000) The role of mixotrophic protists in the population dynamics of the microbial food web in a small artificial pond. Freshwater Biol 43(2):231–241

    Article  Google Scholar 

  • Isaksson A, Bergström AK, Blomqvist P, Jansson M (1999) Bacterial grazing by phagotrophic phytoflagellates in a deep humic lake in northern Sweden. J Plankton Res 21:247–268

    Article  Google Scholar 

  • Izaguirre I, Pizarro H (1998) Epilithic algae in a glacial stream at Hope Bay (Antarctica). Polar Biol 19:24–31

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Izaguirre I, Vinocur A, Mataloni G (1996) Summer changes in vertical distribution of chlorophyll-a in Boeckella Lake (Hope Bay, Antarctic Peninsula). Antarct Record 40:43–52

    Google Scholar 

  • Izaguirre I, Vinocur A, Mataloni G, Pose M (1998) Phytoplankton communities in relation to trophic status in lakes from Hope Bay (Antarctic Peninsula). Hydrobiologia 369(370):73–87

    Article  Google Scholar 

  • Izaguirre I, Mataloni G, Allende L, Vinocur A (2001) Summer fluctuations of microbial planktonic communities in a eutrophic lake – Cierva Point, Antarctica. J Plankton Res 23:1095–1109

    Article  CAS  Google Scholar 

  • Izaguirre I, Allende L, Marinone MC (2003) Comparative study of the planktonic communities from lakes of contrasting trophic status at Hope Bay (Antarctic Peninsula). J Plankton Res 25:1079–1097

    Article  Google Scholar 

  • Izaguirre I, Saad JF, Schiaffino MR, Vinocur A, Tell G, Sánchez ML, Allende L, Sinistro R (2016) Drivers of phytoplankton diversity in Patagonian and Antarctic lakes across a latitudinal gradient (2150 km): the importance of spatial and environmental factors. Hydrobiologia 764:157–170

    Article  CAS  Google Scholar 

  • Izaguirre I, Allende L, Schiaffino MR (2021) Phytoplankton in Antarctic lakes: biodiversity and main ecological features. Hydrobiologia 848:177–207

    Article  Google Scholar 

  • Kamjunke N, Henrichs T, Gaedke U (2007) Phosphorus gain by bacterivory promotes the mixotrophic flagellate Dinobryon spp. during re-oligotrophication. J Plankton Res 29:39–46

    Article  CAS  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klaveness D, Bråte J, Patil V, Shalchian-Tabrizi K, Kluge R, Ragnar Gislerød H, Jakobsen KS (2011) The 18S and 28S rDNA identity and phylogeny of the common lotic chrysophyte Hydrurus foetidus. Eur J Phycol 46:282–291

    Article  Google Scholar 

  • Klaveness D (2017) Hydrurus foetidus (Chrysophyceae): an inland macroalga with potential. J Appl Phycol 29:1485–1491

    Article  CAS  Google Scholar 

  • Kristiansen J (2005) Golden Algae. A Biology of Chrysophytes. A.R.G. Gantner Verlag KG

  • Komárek J, Fott B (1983) Chlorophyceae (Grünalgen), Ordnung: Chlorococcales. In: Huber–Pestalozzi G (ed) Die Binnnengewässer 16/7. E. Schweizerbart´sche Verlagsbuchhandlung, Stuttgart

  • Komárek J, Anagnostidis K (1999) Cyanoprokaryota. I. Chroococcales. In: Ettl H, Gärtner G, Heynig H, Mollenhauer D (eds). Süßwasserflora von Mitteleuropa. Gustav Fischer, Jena Stuttgart Lübeck Ulm, 19/1

  • Komárek J, Anagnostidis K (2005) Cyanoprokaryota. 2. Oscillatoriales. In: Büdel B, Krienitz L, Gärtner G, Schagerl M (eds), Süsswasserflora von Mitteleuropa 19/2, Elsevier/Spektrum, Heidelberg

  • Kruk C (2010) Morphology captures function in phytoplankton. A large-scale analysis of phytoplankton communities in relation to their environment.Thesis Wageningen University

  • Kruk C, Huszar VLM, Peeters ETHM, Bonilla S, Costa L, Lürling M, Reynolds CS, Scheffer M (2010) A morphological classification capturing functional variation in phytoplankton. Freshwater Biol 55:614–627

    Article  Google Scholar 

  • Lara E, Seppey CVW, Garraza GG, Singer D, Quiroga MV, Mataloni G (2015) Planktonic eukaryote molecular diversity: discrimination of minerotrophic and ombrotrophic peatland pools in Tierra del Fuego (Argentina). J Plankton Res 37:645–655

    Article  Google Scholar 

  • Laybourn-Parry J, Marshall WA (2003) Photosynthesis, mixotrophy and microbial plankton dynamics in two high Arctic lakes during summer. Polar Biol 26(8):517–524

    Article  Google Scholar 

  • Laybourn-Parry J, Pearce DA (2007) The biodiversity and ecology of Antarctic lakes: models for evolution. Philos T Roy Soc B 362:2273–2289

    Article  CAS  Google Scholar 

  • Laybourn-Parry J, James MR, McKnigh DM, Priscu J, Spaulding SA, Shiel R (1997) The microbial plankton of Lake Fryxell, southern Victoria Land, Antarctica, during the summers of 1992 and 1994. Polar Biol 17:62–68

    Article  Google Scholar 

  • Laybourn-Parry J, Roberts EC, Bell EM (2000) Mixotrophy as a survival strategy among planktonic protozoa in Antarctic lakes. In: Davison W, Howard-Williams C, Broady P (eds) Antarctic ecosystems: model for a wider ecological understanding. The Caxton Press, Christchurch, pp 33–40

    Google Scholar 

  • Laybourn-Parry J, Marshall WA, Marchant HJ (2005) Flagellate nutritional versatility as a key to survival in two contrasting Antarctic saline lakes. Freshwater Biol 50:830–838

    Article  Google Scholar 

  • Lewis Smith RI (1984) Terrestrial plant biology of the sub-Antarctic and Antarctic. In: Laws RM (ed) 18 Antarctic ecology. Academic Press, London, pp 61–162

    Google Scholar 

  • Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Annu Rev Ecol Evol S 39:615–639

    Article  Google Scholar 

  • Litchman E, Tezanos Pinto P, Klausmeier CA, Thomas MK, Yoshiyama K (2010) Linking traits to species diversity and community structure in phytoplankton. Hydrobiologia 653:15–28

    Article  CAS  Google Scholar 

  • Magurran AE, Henderson PA (2003) Explaining the excess of rare species in natural species abundance distributions. Nature 422:714–716

    Article  CAS  PubMed  Google Scholar 

  • Mahé F, Rognes T, Quince C, de Vargas C, Dunthorn M (2014) Swarm: robust and fast clustering method for amplicon-based studies. PeerJ 2:e593

    Article  PubMed  PubMed Central  Google Scholar 

  • Marshall W, Laybourn-Parry J (2002) The balance between photosynthesis and grazing in Antarctic mixotrophic cryptophytes during summer. Freshwater Biol 47:2060–2070

    Article  Google Scholar 

  • Massana R, Balagué V, Guillou L, Díez B, Pedros-Alió C (2004) Picoeukaryotic diversity in an oligotrophic coastal site studied by molecular and culturing approaches. FEMS Microbiol Ecol 50:231–243

    Article  CAS  PubMed  Google Scholar 

  • Mataloni G, Tesolín G, Sacullo F, Tell G (2000) Factors regulating summer phytoplankton in a highly eutrophic Antarctic lake. Hydrobiologia 432:65–72

    Article  Google Scholar 

  • McKnight DM, Howes BL, Taylor CD, Goehringer DD (2000) Phytoplankton dynamics in a stably stratified Antarctic lake during winter darkness. J Phycol 36:852–861

    Article  CAS  Google Scholar 

  • McWilliam H, Li WZ, Uludag M, Squizzato S, Park YM, Buso N et al (2013) Analysis Tool Web Services from the EMBL-EBI. Nucleic Acids Res 41:W597–W600

    Article  PubMed  PubMed Central  Google Scholar 

  • Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499

    Article  CAS  PubMed  Google Scholar 

  • Nicholls KH, Wujek DE (2003) Chrysophycean algae. In: Wehr JD, Sheath RG (eds) Freshwater algae of North America. Academic Press, New York, USA, pp 471–509

    Chapter  Google Scholar 

  • Nolte V, Pandey RV, Jost S, Medinger R, Ottenwalder B, Boenigk J, Schlötterer C (2010) Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity. Mol Ecol 19:2908–2915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olrik K (1998) Ecology of mixotrophic flagellates with special reference to Chrysophyceae in Danish lakes. Hydrobiologia 369(370):329–338

    Article  Google Scholar 

  • Padisák J, Crossetti LO, Naselli-Flores L (2009) Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia 621:1–19

    Article  Google Scholar 

  • Pålsson C, Granéli W (2003) Diurnal and seasonal variations in grazing by bacterivorous mixotrophs in an oligotrophic clearwater lake. Arch Hydrobiol 157(3):289–307

    Article  Google Scholar 

  • Pearce DA, Galand PE (2008) Microbial biodiversity and biogeography. In: Vincent W, Laybourn-Parry J (eds) Polar lakes and rivers, limnology of arctic and antarctic aquatic ecosystems. Oxford University Press, New York, pp 213–230

    Chapter  Google Scholar 

  • Priddle J, Hawes I, Ellis-Evans JC, Smith TC (1986) Antarctic aquatic ecosystems as habitats for phytoplankton. Biol Rev 61:199–238

    Article  Google Scholar 

  • Remias D, Jost S, Boenigk J, Wastian J, Lütz C (2013) Hydrurus-related golden algae (Chrysophyceae) cause yellow snow in polar summer snowfields. Phycol Res 61:277–285

    Article  CAS  Google Scholar 

  • Reynolds CS (1997) Vegetation processes in the pelagic: A model for ecosystem theory. Excellence in Ecology, 9. Ecology Institute, Oldendorf/Luhe

  • Reynolds CS (2006) The ecology of phytoplankton. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Reynolds CS, Huszar V, Kruk C, Naselli-Flores L, Melo S (2002) Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24:417–428

    Article  Google Scholar 

  • Rippka R, Coursin T, Hess W, Lichtle C, Scanlan DJ, Palinska KA, Iteman I, Partensky F, Houmard J, Herdman M (2000) Prochlorococcus marinus Chisholm et al, 1992 subsp pastoris subsp nov strain PCC 9511, the first axenic chlorophyll a(2)/b(2)-containing cyanobacterium (Oxyphotobacteria). Int J Syst Evol Microbiol 50:1833–47

    Article  CAS  PubMed  Google Scholar 

  • Rottberger J, Gruber A, Boenigk J, Kroth PG (2013) Influence of nutrients and light on autotrophic, mixotrophic and heterotrophic freshwater chrysophytes. Aquat Microb Ecol 71:179–191

    Article  Google Scholar 

  • Saad J, Unrein F, Tribelli PM, López N, Izaguirre I (2016) Influence of lake trophic conditions on the dominant mixotrophic algal assemblages. J Plankton Res 38:818–829

    Article  CAS  Google Scholar 

  • Salmaso N, Naselli-Flores L, Padisák J (2015) Functional classification and their application in phytoplankton ecology. Freshwater Biol 60:603–619

    Article  Google Scholar 

  • Sanders RW, Porter KG (1988) Phagotrophic phytoflagellates. Adv Microb Ecol 10:167–192

    Article  Google Scholar 

  • Sanders RW, Porter KG, Bennett SJ, DeBiase AE (1989) Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol Oceanogr 34(4):673–687

    Article  Google Scholar 

  • Sanders RW, Porter KG, Caron DA (1990) Relationship between phototrophy and phagotrophy in the mixotrophic chrysophyte Poterioochromonas malhamensis. Microb Ecol 19:97–109

    Article  CAS  PubMed  Google Scholar 

  • Sandgren CD (1988) The ecology of chrysophyte flagellates: their growth and perennation strategies as freshwater phytoplankton. En: Sandgren, CD (ed), Growth and reproductive strategies of freshwater phytoplankton. Cambridge University Press, Nueva York Melbourne Sydney

  • Savin MC, Martin JL, LeGresley M, Giewat M, Roonye-Varga J (2004) Plankton diversity in the Bay of Fundy as measured by morphological and molecular methods. Microb Ecol 48:51–65

    Article  CAS  PubMed  Google Scholar 

  • Schaefer CEGR, Pereira TTC, Ker JC, Almeida ICC, Simas FNB, de Oliveira FS, Corrêa GR, Vieira G (2015) Soils and landforms at Hope Bay, Antarctic Peninsula: formation, classification, distribution and relationships. Soil Sci Soc Am J 79:175–184

    Article  CAS  Google Scholar 

  • Schiaffino MR, Unrein F, Gasol JM, Massana R, Balagué V, Izaguirre I (2011) Bacterial community structure in a latitudinal gradient of lakes: the roles of spatial versus environmental factors. Freshwater Biol 56:1973–1991

    Article  Google Scholar 

  • Schiaffino MR, Lara E, Fernández LD, Balagué V, Singer D, Seppey CW, Massana R, Izaguirre I (2016) Microbial eukaryote communities exhibit robust biogeographical patterns along a gradient of Patagonian and Antarctic lakes. Environ Microbiol 18(12):5249–5264

    Article  CAS  PubMed  Google Scholar 

  • Schmidtke A, Bell EM, Weithoff G (2006) Potential grazing impact of the mixotrophic flagellate Ochromonas sp. (Chrysophyceae) on bacteria in an extremely acidic lake. J Plankton Res 28:991–1001

    Article  CAS  Google Scholar 

  • Singer D, Metz S, Unrein F, Shimano S, Mazei Y, Mitchell EAD, Lara E (2019) Contrasted micro-eukaryotic diversity associated with Sphagnum mosses in tropical, subtropical and temperate climatic zones. Microbial Ecol. https://doi.org/10.1007/s00248-019-01325-7

    Article  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Starmach K (1985) Chrysophyceae und Haptophyceae. Gustav Fischer Verlag, Stuttgart, New York

    Google Scholar 

  • Scoble JM, Cavalier-Smith T (2014) Scale evolution in Paraphysomonadida (Chrysophyceae): Sequence phylogeny and revised taxonomy of Paraphysomonas, new genus Clathromonas, and 25 new species. Eur J of Protistol 50:551–592

    Article  Google Scholar 

  • Thouvenot A, Richardot M, Debroas D, Devaux J (1999) Bacterivory of metazooplankton, ciliates and flagellates in a newly flooded reservoir. J Plankton Res 21(9):1659–1679

    Article  Google Scholar 

  • Unrein F, Izaguirre I, Massana R, Balagué V, Gasol JM (2005) Nanoplankton assemblages in maritime Antarctic lakes: characterisation and molecular fingerprinting comparison. Aquat Microb Ecol 40:269–282

    Article  Google Scholar 

  • Unrein F, Massana R, Alonso-Sáez L, Gasol JM (2007) Significant year-round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system. Limnol Oceanogr 52:456–469

    Article  Google Scholar 

  • Unrein F, Gasol JM, Massana R (2010) Dinobryon faculiferum (Chrysophyta) in coastal Mediterranean seawater: presence and grazing impact on bacteria. J Plankton Res 32:559–564

    Article  Google Scholar 

  • Utermöhl M (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt int Ver Theor Angew Limnol 9:1–38

    Google Scholar 

  • Velasco-González I, Sanchez-Jimenez A, Singer D, Murciano A, Díez-Hermano S, Lara E, Martín-Cereceda M (2020) Rain-fed granite rock basins accumulate a high diversity of dormant microbial eukaryotes. Microb Ecol 79:882–897

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Vinocur A, Unrein F (2000) Typology of lentic water bodies at Potter Peninsula (King George Island, Antarctica) based on physical-chemical characteristics and phytoplankton communities. Polar Biol 23:858–870

    Article  Google Scholar 

  • Wall DH, Virginia RA (1999) Controls on soil biodiversity: Insights from extreme environments. Appl Soil Ecol 13:137–150

    Article  Google Scholar 

  • Weithoff G (2003) The concepts of ‘plant functional types’ and ‘functional diversity’ in lake phytoplankton- a new understanding of phytoplankton ecology? Freshwater Biol 48:1669–1675

    Article  Google Scholar 

  • Wilken S, Schuurmans JM, Matthijs HC (2014) Do mixotrophs grow as photoheterotrophs? Photophysiological acclimation of the chrysophyte Ochromonas danica after feeding. New Phytol 204:882–889

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The Antarctic expeditions were supported by the Dirección Nacional del Antártico (DNA) of Argentina, within the framework of a cooperative project between this institution, University of Buenos Aires and the Institut de Ciències del Mar (ICM)-CSIC. The investigations were financed by grants of the Argentinean Funds for Technical and Scientific Investigation (FONCYT, PICT 04440 and PICT 32732); the Spanish projects MIXANTAR (REN2002-11396-E/ANT) and MICRODIFF (DGICYT REN2001-2120/MAR) grant SB2001-0166 from the Spanish MECyD; the grant "Atracción de talento investigador" from the Community of Madrid (2017-T1/AMB- 5210); and the Swiss NSF (P2NEP3-178543). We wish to thank the members of the Argentinian Esperanza Station for the logistic support. We also thank Dr. Elie Verleyen and other two anonymous reviewers for their valuable comments for improving the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

II, FU conceived and designed research, conducted the field work and experiments, performed the clone libraries and wrote the manuscript; MRS and VB contributed with the molecular analyses and their data analyses; EL, DS performed the Illumina data analyses; JG contributed with the research design and with funding; RM performed the phylogenetic analyses, contributed with the research design and with funding. All authors contributed to the writing of the manuscript and approved it.

Corresponding author

Correspondence to Irina Izaguirre.

Ethics declarations

Conflict of interest

There are not any conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Izaguirre, I., Unrein, F., Schiaffino, M.R. et al. Phylogenetic diversity and dominant ecological traits of freshwater Antarctic Chrysophyceae. Polar Biol 44, 941–957 (2021). https://doi.org/10.1007/s00300-021-02850-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-021-02850-3

Keywords

Navigation