Abstract—
Species diversity of phototrophic eukaryotes (PEs) with cell size <3 µm in autumn phytoplankton of the Kara and Laptev seas was studied. High-throughput sequencing of the 18S rRNA gene V4 region revealed 15 classes of algae in the plankton pico-sized fraction, which belonged to five divisions: Haptophyta, Cryptophyta, Chlorophyta, Ochrophyta, and Dinoflagellata. Dinoflagellata and green algae of the class Mamiellophyceae were the main contributors to total PE sequences. Chlorophyta was the most diverse section, represented by seven classes: Mamiellophyceae, Trebouxiophyceae, Nephroselmidophycea, Palmophyllophyceae, Pyramimonadophyceae, Chlorodendrophyceae, and Chlorophyceae. Bolidophyceaea species Triparma strigata and T. laevis, as well as the diatom Skeletonema marinoi, were first identified in the Kara and Laptev Seas, respectively. The hydrological conditions on the stations determined the PE taxonomic composition. The diversity indices were higher at the stations located in the upper estuary of river Khatanga and at the areas of both seas adjacent to the Khatanga and Ob estuaries than at the northernmost Laptev Sea station. The obtained data showed that the taxonomic composition of the smallest phytoplankton fraction of the two shelf seas of the Russian Arctic was similar to that found in other Arctic regions.
Similar content being viewed by others
REFERENCES
Balzano, S., Marie, D., Gourvil, P., and Vaulot, D., Com-position of the summer photosynthetic pico and nano-plankton communities in the Beaufort Sea assessed by T-RFLP and sequences of the 18S rRNA gene from flow cytometry sorted samples, ISME J., 2012, vol. 6, pp. 1480–1498.
Belevich, T.A., Demidov, A.B., Makkaveev, P.N., Shchuka, S.A., and Flint, M.V., Picophytoplankton distribution along Khatanga Bay-shelf-continental slope environment gradients in the western Laptev Sea, Heliyon, 2021b, vol. 7, e06224, pp. 1–9.
Belevich, T.A., Ilyash, L.V., Arashkevich, E.G., and Flint, M.V., Picophytoplankton of the Laptev Sea in autumn, Doklady Earth Sci., 2019a, vol. 484, no. 2, pp. 207–210.
Belevich, T.A., Ilyash, L.V., Demidov, A.B., and Flint, M.V., Picophytoplankton distribution at the Ob river section and in the western part of the Kara Sea, Oceanology, 2019, vol. 59, pp. 871‒880.
Belevich, T.A., Milyutina, I.A., Abyzova, G.A., and Troitsky, A.V., The pico-sized Mamiellophyceae and a novel Bathycoccus clade from the summer plankton of Russian Arctic Seas and adjacent waters, FEMS Microbiol. Ecol., 2021a, vol. 97, art. fiaa251.
Belevich, T.A., Milyutina, I.A., Troitsky, A.V., and Flint, M.V., Picophytoplankton in Blagopoluchia Bay (Novaya Zemlya Archipelago) and adjacent part of the Kara Sea, Oceanology, 2020, vol. 60, pp. 473‒482.
Belevich, T.A., Ilyash, L.V., Milyutina, I.A., Logacheva, M.D., Goryunov, D.V., and Troitsky, A.V., Photosynthetic picoeukaryotes in the land-fast ice of the White Sea, Russia, Microb. Ecol., 2018, vol. 75, pp. 582–597.
Callahan, B.J., McMurdie, P.J., Rosen, M.J., McMurdie, P.J., and Holmes, S.P., Bioconductor workflow for microbiome data analysis: from raw reads to community analyses, [version 2; peer review: 3 approved], F1000Research, 2016. 5, pp. 1492–1541.
Clarke, K.R. and Gorley, R.N., PRIMER v6.: User Manual/Tutorial, Plymouth: PRIMER-E, 2006.
Demidov, A.B., Sukhanova, I.N., Belevich, T.A., Flint, M.V., Gagarin, V.I., Sergeeva, V.M., Eremeeva, E.V., and Fedorov, A.V., Size-fractionated surface phytoplankton in the Kara and Laptev seas: environmental control and spatial variability, Mar. Ecol. Progr. Ser., 2021, vol. 664, pp. 59–77.
Gordeev, V.V., Martin, J.M., Sidorov, I.S., and Sidorova, M.V., A reassessment of the Eurasian river input of water, sediment, major elements, and nutrients to the Arctic Ocean, Amer. J. Sci., 1996, vol. 296, pp. 664–691.
Hammer, Ø., Harper, D.A.T., and Ryan, P.D., 2001. Past: Paleontological Statistics Software Package for Education and Data Analysis, Palaeontol. Electron., 2001, vol. 4, art. 4, pp. 1–9.
Ichinomiya, M., Lopes dos Santos, A., Gourvil, P., Yoshikawa, S., Kamiya, M., Ohki, K., Audic, S., de Vargas, C., Noel, M.-H., Vaulot, D., and Kuwata, A., Diversity and oceanic distribution of the Parmales (Bolidophyceae), a picoplanktonic group closely related to diatoms, ISME J., 2016, vol. 10, pp. 2419–2434.
Joli, N., Gosselin, M., Ardyna, M., Babin, M., Onda, D.F., Tremblay, J.-É., and Lovejoy, C., Need for focus on microbial species following ice melt and changing freshwater regimes in a Janus Arctic Gateway, Sci. Rep., 2018, vol. 8, art. 9405.
Kilias, E.S., Nöthig, E.-M., Wolf, C., and Metfies, K., Picoeukaryote plankton composition of West Spitsbergen at the entrance to the Arctic Ocean, J. Eukaryot. Microbiol., 2014, vol. 61, pp. 569–579.
Kilias, E., Wolf, C., Nöthig, E.-M., Peeken, I., and Metfies, K., Protist distribution in the western Fram Strait in summer 2010 based on 454-pyrosequencing of 18S r-DNA, J. Phycol., 2013, vol. 49, pp. 996–1010.
Kirkham, A.R., Lepère, C., Jardillier, L.E., Not, F., Bouman, H., Mead, A., and Scanlan, D.J., A global perspective on marine photosynthetic picoeukaryote community structure, ISME J., 2013, vol. 7, pp. 922–936.
LaJeunesse, T.C., Lambert, G., Anderson, R.A., Coffroth, M.A., and Galbraith, D.W., Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates, J. Phycol., 2005, vol. 41, pp. 880–886.
Lin, S., Zhang, H., Hou, Y., Miranda, L., and Bhattacharya, D., Development of a dinoflagellate-oriented PCR primer set leads to detection of picoplanktonic dinoflagellates from Long Island Sound, Appl. Environ. Microbiol., 2006, vol. 72, pp. 5626–5630.
Majaneva, M., Rintala, J.M., Piisila, M., Fewer, D.P., and Blomster, J., Comparison of wintertime eukaryotic community from sea ice and open water in the Baltic Sea, based on sequencing of the 18S rRNA gene, Polar Biol., 2012, vol. 35, pp. 875–889.
Makarevich, P., Druzhkova, E., and Larionov, V., Primary producers of the Barents Sea, diversity of ecosystems, in Diversity of Ecosystems, Mahamane A., Ed., InTech, 2012, pp. 367–392.
Metfies, K., von Appen, W.-J., Kilias, E., Nicolaus, A., and Nöthig, E.-M., Biogeography and photosynthetic biomass of Arctic marine pico-eukaryotes during summer of the record sea ice minimum 2012, PLoS One, 2016, vol. 11. e0148512, pp. 1–20.
Moon-van der Staay, S.Y., De Wachter, R., and Vaulot, D., Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity, Nature, 2001, vol. 409, pp. 607–610.
Sergeeva, V.M., Sukhanova, I.N., Flint, M.V., Polu-hin, A.A., Kremenetskiy, V.V., Fedorov, A.V., Lange, E.K., Shchuka, S.A., Sakharova, E.G., and Georgieva, E.U., Phytoplankton of the St. Anna Trough: influence of abiotic factors, Oceanology, 2020, vol. 60, pp. 458–472.
Sørensen, N., Daugbjerg, N., and Richardson, K., Choice of pore size can introduce artefacts when filtering Picoeukaryotes for molecular biodiversity studies, Microb. Ecol., 2013, vol. 65, pp. 964–968.
Stain, R., Circum Arctic river discharge and its geological record, Int. J. Earth Sci., 2000, vol. 89, pp. 447–449.
Sukhanova, I.N., Flint, M.V., and Sergeeva, V.M., Phytoplankton of the surface desalted lens of the Kara Sea, Oceanology, 2012, vol. 52, pp. 635‒645.
Sukhanova, I.N., Flint, M.V., Artemyev, V.A., Makkaveev, P.N., Nedospasov, A.A., Fedorov, A.V., and Sakharova, E.G., Phytoplankton of the Khatanga Bay, shelf and continental slope of the western Laptev Sea, Oceanology, 2019, vol. 59, pp. 648–657.
Sukhanova, I.N., Flint, M.V., Mosharov, S.A., and Sergeeva, V.M., Structure of the phytoplankton communities and primary production in the Ob River estuary and over the adjacent Kara Sea Shelf, Oceanology, 2010, vol. 50, pp. 743‒758.
Sukhanova, I.N., Flint, M.V., Sazhin, A.F., Serge-eva, V.M., and Druzhkova, E.I., Phytoplankton in the northwestern Kara Sea, Oceanology, 2015, vol. 55, pp. 547‒560.
Terrado, R., Scarcella, K., Thaler, M., Vincent, W.F., and Lovejoy, C., Small phytoplankton in Arctic seas: vulnerability to climate change, Biodiversity, 2013, vol. 14, pp. 2–18.
Tragin, M. and Vaulot, D., Novel diversity within marine Mamiellophyceae (Chlorophyta) unveiled by metabarcoding, Sci. Rep., 2019, vol. 9, art. 5190.
Tremblay, G., Belzile, C., Gosselin, M., Poulin, M., Roy, S., and Tremblay, J.-É., Late summer phytoplankton distribution along a 3500 km transect in Canadian Arctic waters: strong numerical dominance by picoeukaryotes, Aquat. Microb. Ecol., 2009, vol. 54, pp. 55–70.
Vaulot, D., Eikrem, W., Viprey, M., and Moreau, H., The diversity of small eukaryotic phytoplankton (≤3 µm) in marine ecosystems, FEMS Microbiol. Rev., 2008, vol. 32, pp. 795–820.
Worden, A.Z., Picoeukaryote diversity in coastal waters of the Pacific Ocean, Aquat. Microb. Ecol., 2006, vol. 43, pp. 165–175.
Zhang, F., He, J., Lin, L., and Jin, H., Dominance of picophytoplankton in the newly open surface water of the central Arctic Ocean, Polar Biol., 2015, vol. 38, pp. 1081–1089.
Zhu, F., Massana, R., Not, F., Marie, D., and Vaulot, D., Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene, FEMS Microbiol. Ecol., 2005, vol. 52, pp. 79–92.
Funding
The work was carried out within the framework of the State Assignment of the Lomonosov Moscow State University part 2 (topic nos. 121032300135-7 and АААА-А17-117120540067-0) and of the Future of the Planet and Global Environmental Changes Program for Development of Interdisciplinary Scientific and Educational School of the Moscow State University and was supported by the Russian Foundation for Basic Research, project no. 19-05-00026.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Translated by P. Sigalevich
Rights and permissions
About this article
Cite this article
Belevich, T.A., Milyutina, I.A. Species Diversity of Phototrophic Picoplankton in the Kara and Laptev Seas. Microbiology 91, 67–76 (2022). https://doi.org/10.1134/S0026261722010027
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0026261722010027