Structure and Functioning of Plankton Communities of Phototrophic and Mixotrophic Protists in the Coastal Lagoon “Lake Kislo-Sladkoe” (White Sea, Karelian Coast)
https://doi.org/10.31857/S2587556622060127
Abstract
For the first time the taxonomic composition and vertical structure of phototrophic protist (PhP) communities were determined in a meromictic water body of the Russian coast of the Arctic, namely a lagoon Lake Kislo-Sladkoe, using DNA metabarcoding. Temperature, salinity, oxygen concentration, pH, Eh, illumination, and functional parameters of chlorophyll fluorescence were measured at different depths. 140 operational taxonomic units of PhP belonging to major taxa Dinoflagellata, Chlorophyta, Cryptophyta, Haptophyta, Ochrophyta, Cercozoa were identified. PP predominated over heterotrophic protists at depths of 0– 1.0 and 2.5–3.5 m reaching a maximum in the chemocline, especially in the 3.0 m horizon, above the redox transition. The taxonomic composition of the PhP in different layers differed according to the hydrological and hydrochemical stratification. In addition to abiotic factors, the composition and distribution of PP was influenced by predatory protists such as the cercozoan flagellate Ebria tripartita and the dinoflagellate Oxyrrhis marina, which significantly reduced the abundance of PhP while their mass distribution. Five layers were identified with different sets of dominant PhP. The surface 0−0.5 m layer of freshened water was featured the dominance of cryptophytes Teleaulax sp. and Hemiselmis cryptochromatica. The photosynthesis activity here was lower compared to the underlying layers that may be determined by photoinhibition. In the 1.0–2.0 m layer of seawater below the pycnocline Chlorophyta dominated, which are typical for picoplankton of the northern seas, as well as representatives of Cryptophyta, Haptophyta, Pedinellida, and diatoms. The PhP community at the lower boundary of the oxycline (2.5 m) had a specific structure with the mass development of the mixotrophic dinoflagellate Heterocapsa rotundata, for which the most favorable conditions were formed here facilitating the transition from photosynthesis to phagotrophic consumption of bacteria. In the chemocline, a maximum of chlorophyll was recorded, which was formed by cryptophyte Rhodomonas sp., demonstrating high rates of photosynthesis efficiency, despite the presence of hydrogen sulfide and low illumination. In the deeper anaerobic zone, cysts and DNA of dead protists were preserved apparently, whereas the remains of the protist cells settled in the bottom layer.
Keywords
About the Authors
A. O. PlotnikovRussian Federation
Orenburg
E. A. Selivanova
Russian Federation
Orenburg
Yu. A. Khlopko
Russian Federation
Orenburg
D. A. Voronov
Russian Federation
Moscow
D. N. Matorin
Russian Federation
Moscow
D. A. Todorenko
Russian Federation
Moscow
E. D. Krasnova
Russian Federation
Moscow
References
1. Abad D., Albaina A., Aguirre M., Laza-Martínez A., Uriarte I., Iriarte A., Villate F., Estonba A. Is metabarcoding suitable for estuarine plankton monitoring? A comparative study with microscopy. Mar. Biol., 2016, vol. 163, no. 7, 149. https://doi.org/10.1007/s00227-016-2920-0
2. Baatar B., Chiang P.-W., Rogozin D.Y., Wu Y.-T., Tseng C.-H., Yang C.-Y., Chiu H.-H., Oyuntsetseg B., Degermendzhy A.G., Tang S.-L. Bacterial communities of three saline meromictic lakes in Central Asia. PLOS ONE, 2016, vol. 11, no. 3, e0150847. https://doi.org/10.1371/journal.pone.0150847
3. Belevich T., Il’yash L. The seasonal dynamic of picophytoplankton primary production in the Kandalaksha Bay, the White Sea. In Tr. 7 mezhdunar. nauchn.-prakt. konf. MARESEDU-2018 [Proc. 7 Int. Conf. MARESEDU2018]. Tver’: PoliPRESS, vol. 4, 2019, pp. 193–196. (In Russ.).
4. Belevich T.A., Milyutina I.A. Species diversity of phototrophic picoplankton in the Kara and Laptev seas. Microbiol., 2022, vol. 91, no. 1, pp. 67–76. https://doi.org/10.1134/S0026261722010027
5. Bel’kova N.L. Molecular genetic methods for the analysis of microbial communities. In Raznoobrazie mikrobnkykh soobshchestv vnutrennikh vodoemov Rossii: uchebno-metodicheskoe posobie [Diversity of Microbial Communities of Inland Waters in Russia: Handbook]. Yaroslavl: Printhhauz Publ., 2009, pp. 53‒63. (In Russ.).
6. Casamayor E.O., Schafer H., Baneras L., Pedros-Alio C., Muyzer G. Identification of and spatio-temporal differences between microbial assemblages from two neighboring sulfurous lakes: comparison by microscopy and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol., 2000, vol. 66, no. 2, pp. 499–508. https://doi.org/10.1128/aem.66.2.499-508.2000
7. Chekanov K.A., Krasnova E.D. Characteristics of the photosynthetic apparatus of crytophyte flagellates Rhodomonas sp. from the chemocline of a stratified lagoon at the cape Zeleny (White Sea, Kandalaksha Bay). In Mater. 22 mezhdunar. nauchn. konf. (Shkoly) po morskoi geologii “Geologiya morei i okeanov” [Geology of Seas and Oceans. Proc. 22 Int. Conf. on Marine Geology]. Moscow: Instit. of Oceanology of RAS, vol. 3, 2019, pp. 232–234. (In Russ.).
8. Del Campo J., Pizzorno A., Djebali S., Bouley J., Haller M., Pérez-Vargas J., Lina B., Boivin G., Hamelin M.-E., Nicolas F., Le Vert F., Leverrier Y., Rosa-Calatrava M., Marvel J., Hill F. OVX836 a recombinant nucleoprotein vaccine inducing cellular responses and protective efficacy against multiple influenza A subtypes. NPJ Vaccines, 2019, vol. 4, no. 4. https://doi.org/10.1038/s41541-019-0098-4
9. Dzhembekova N., Moncheva S., Ivanova P., Slabakova N., Nagai S. Biodiversity of phytoplankton cyst assemblages in surface sediments of the Black Sea based on metabarcoding. Biotechnol. Biotechnol. Equip., 2018, vol. 32, no. 6, pp. 1507–1513. https://doi.org/10.1080/13102818.2018.1532816
10. Edgar R.C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 2010, vol. 26, no. 19, pp. 2460–2461. https://doi.org/10.1093/bioinformatics/btq461
11. Edgar R.C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods, 2013, vol. 10, pp. 996‒998. https://doi.org/10.1038/nmeth.2604
12. Falkowski P.G., Raven J.A. Aquatic Photosynthesis. USA: Princeton Univ. Press, 2007. 488 p.
13. Gorlenko V.M., Vainstein M.B., Kachalkin V.I. Microbiological characteristic of lake Mogilnoye. Arch. Hydrobiol., 1978, vol. 81, no 4, pp. 475−492.
14. Gran-Stadniczeñko S., Egge E., Hostyeva V., Logares R., Eikrem W., Edvardsen B. Protist diversity and seasonal dynamics in Skagerrak plankton communities as revealed by metabarcoding and microscopy. J. Eukaryot. Microbiol., 2018, vol. 66, no. 3, pp. 494−513. https://doi.org/10.1111/jeu.12700
15. Guillou L., Bachar D., Audic S. et al. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy. Nucleic Acids Res., 2013, vol. 41, no. D1, pp. D597–D604. https://doi.org/10.1093/nar/gks1160
16. Hakala A. Meromixis as a part of lake evolution – observations and a revised classification of true meromictic lakes in Finland. Boreal Environ. Res., 2004, vol. 9, pp. 37–53.
17. Ilyash L.V., Radchenko I.G., Kuznetsov L.L., Lisitzin A.P., Martynova D.M., Novigatsky A.N., Tchultsova A.L. Spatial variability of the species composition, abundance, and productivity of the phytoplankton in the White sea in the late summer period. Oceanol., 2011, vol. 51, pp. 19–26. https://doi.org/10.1134/S000143701101005X
18. İnceoğlu Ö., Llirós M., Crowe S.A. et al. Vertical distribution of functional potential and active microbial communities in meromictic lake Kivu. Microb. Ecol., 2015, vol. 70, no. 3, pp. 596–611. https://doi.org/10.1007/s00248-015-0612-9
19. Jeunen G., Lamare M.D., Knapp M. et al. Water stratification in the marine biome restricts vertical environmental DNA (eDNA) signal dispersal. Environmental DNA, 2019, vol. 2, pp. 99–111. https://doi.org/10.1002/edn3.49
20. Krasnova E., Matorin D., Belevich T., Efimova L., Kharcheva A., Kokryatskaya N., Losyuk G., Todorenko D., Voronov D., Patsaeva S. The characteristic pattern of multiple colored layers in coastal stratified lakes in the process of separation from the White Sea. Chin. J. Oceanol. Limnol., 2018, no. 6, pp. 1–16. https://doi.org/10.1007/s00343-018-7323-2
21. Krasnova E.D. Ecology of Meromictic Lakes of Russia. 1. Coastal marine waterbodies. Water Resour., 2021, vol. 48, no. 3, pp. 427–438. https://doi.org/10.1134/S009780782103009X
22. Krasnova E.D., Pantyulin A.N., Matorin D.N., Todorenko D.A., Belevich T.A., Milyutina I.A., Voronov D.A. Blooming of the cryptomonad alga Rhodomonas sp. (Cryptophyta, Pyrenomonadaceae) in the redox zone of the basins separating from the White sea. Microbiol., 2014, vol. 83, pp. 270–277. https://doi.org/10.1134/S0026261714030102
23. Krasnova E.D., Voronov D.A., Demidenko N.A., Kokryatskaya N.M., Pantyulin A.N., Rogatykh T.A., Samsonov T.E., Frolova N.L., Shaporenko S.I. For inventory of relict basins separated from the White Sea. In Kompleksnye issledovaniya Babiego morya, polu-izolirovannoi belomorskoi laguny: geologiya, gidrologiya, biota [Integrated Research of the Babie More, Semi-Isolated White-Sea Lagoon: Geology, Hydrology, Biota]. Tr. Belomorskoi biostantsii MGU [Proc. White Sea Biol. Station of MSU], vol. 12. Moscow: KMK Publ., 2016, pp. 211–241. (In Russ.).
24. Lauro F.M., DeMaere M.Z., Yau S., Brown M.V., Ng C., Wilkins D., Raftery M.J., Gibson J.A., AndrewsPfannkoch C., Lewis M., Hoffman J.M., Thomas T., Cavicchioli R. An integrative study of a meromictic lake ecosystem in Antarctica. ISME J., 2010, vol. 5, pp. 879–895. https://doi.org/10.1038/ismej.2010.185
25. Lewis W.M., Jr. A revised classification of lakes Based on Mixing. Can. J. Fish. Aquat. Sci., 1983, vol. 40, pp. 1779−1787. https://doi.org/10.1139/f83-207
26. Losyuk G.N., Kokryatskaya N.M., Krasnova E.D. Hydrogen sulfide contamination of coastal lakes at different stages of isolation from the White sea. Oceanol., 2021, vol. 61, pp. 351–361. https://doi.org/10.1134/S0001437021020120
27. Lunina O.N., Savvichev A.S., Krasnova E.D., Kokryatskaya N.M., Veslopolova E.F., Kuznetsov B.B., Gorlenko V.M. Succession processes in the anoxygenic phototrophic bacterial community in lake Kislo-Sladkoe (Kandalaksha Bay, White Sea). Microbiol., 2016, vol. 85, pp. 531–544. https://doi.org/10.1134/S0026261716050118
28. Matorin D., Antal T., Ostrowska M., Rubin A., Ficek D., Majchrowski R. Chlorophyll fluorimetry as a method for studying light absorption by photosynthetic pig ments in marine algae. Oceanol., 2004, vol. 46, no. 4, pp. 519–531.
29. Matorin D.N., Rubin A.B. Fluorestsentsii khlorofilla vysshikh rastenii i vodoroslei [Chlorophyll Fluorescence of Higher Plants and Algae]. Moscow, Izhevsk, 2012. (In Russ.).
30. Millette N.C., Pierson J.J., Aceves A., Stoecker D.K. Mixotrophy in Heterocapsa rotundata: A mechanism for dominating the winter phytoplankton. Limnol. Oceanogr., 2017, vol. 62, iss. 2, pp. 836–845. https://doi.org/10.1002/lno.10470
31. Mordasova N.V. Indirect estimation of water productivity by the chlorophyll content. Tr. VNIRO, 2014, vol. 152, p. 41‒56. (In Russ.).
32. Netsvetaeva O.P., Makedonskaya I.Y., Korobov V.B., Zmetnaya M.I. Dependence of oxygen saturation on the “a” chlorophyll content in the surface layer of the White Sea. Arktika: Ekol. Ekon., 2018, vol. 31, no. 3, рр. 31‒41. (In Russ.). https://doi.org/10.25283/2223-4594-2018-3-31-41
33. Orsi W., Song Y.C., Hallam S., Edgcomb V. Effect of oxygen minimum zone formation on communities of marine protists. ISME J., 2012, vol. 6, pp. 1586–1601. https://doi.org/10.1038/ismej.2012.7
34. Romanenko F.A., Shilova O.S. The postglacial uplift of the Karelian Coast of the White Sea according to radiocarbon and diatom analyses of lacustrine boggy deposits of Kindo Peninsula. Dokl. Earth Sci., 2012, vol. 442, part 2, pp. 242–246. https://doi.org/10.1134/S1028334X12020079
35. Salmaso N. Effects of habitat partitioning on the distribution of bacterioplankton in deep lakes. Front. Microbiol., 2019, vol. 10, 2257. https://doi.org/10.3389/fmicb.2019.02257
36. Savvichev A.S., Babenko V.V., Lunina O.N., Letarova M.A., Boldyreva D.I., Veslopolova E.F., Demidenko N.A., Kokryatskaya N.M., Krasnova E.D., Gaisin V.A., Kostryukova E.S., Gorlenko V.M., Letarov A.V. Sharp water column stratification with an extremely dense microbial population in a small meromictic lake, Trekhtzvetnoe. Environ. Microbiol., 2018, vol. 20, no. 10, pp. 3784‒3797. https://doi.org/10.1111/1462-2920.14384
37. Savvichev A.S., Kadnikov V.V., Rusanov I.I. et al. Microbial processes and microbial communities in the water column of the polar meromictic lake Bol’shie Khruslomeny at the White Sea coast. Front. Microbiol., 2020, vol. 11, 01945. https://doi.org/10.3389/fmicb.2020.01945
38. Savvichev A.S., Lunina O.N., Rusanov I.I., Zakharova E.E., Veslopolova E.F., Ivanov M.V. Microbiological and isotopic geochemical investigation of Lake Kislo-Sladkoe, a meromictic water body at the Kandalaksha Bay shore (White Sea). Microbiol., 2014, vol. 83, pp. 56–66. https://doi.org/10.1134/s0026261714010111
39. Schreiber U. Pulse-Amplitude-Modulation (PAM) Fluorymetry and Saturation Pulse Method: An Overview In Chlоrоphyll A Fluоrescence: A Signature оf Phоtоsynthesis. Gоvindjee G., Papageоrgiоu G., Eds. Dоrdrecht: Springer, 2004, pp. 279–319. https://doi.org/10.1007/978-1-4020-3218-9
40. Selivanova E.A., Ignatenko M.E., Yatsenko-Stepanova T.N., Plotnikov A.O. Diatom assemblages of the brackish Bolshaya Samoroda River (Russia) studied via light microscopy and DNA metabarcoding. Protistology, 2019, vol. 13, no. 4, pp. 215–235. https://doi.org/10.21685/1680-0826-2019-13-4-5
41. Shaporenko S.I., Koreneva G.A., Pantyulin A.N., Pertsova N.M. Characteristics of the Ecosystems of Water Bodies Separating from Kandalaksha Bay of the White Sea. Water Resour., 2005, vol. 32, no. 5, pp. 469–483. https://doi.org/10.1007/s11268-005-0060-x
42. Suggett D.J., Prašil О., Bоrоwitzka M.A. Chlоrоphyll a Fluоrescence in Aquatic Sciences: Methоds and Applicatiоns. Dordrecht: Springer, 2011. 326 p. https://doi.org/10.1007/978-90-481-9268-7
43. Todorenko D.A., Krasnova E.D., Matorin D.A. Study of the functional state of the photosynthetic apparatus of phytoplankton in the separated water bodies on the White Sea coast by using fluorescence methods. In Tr. 7 Mezhdunar. nauchn.-prakt. konf. MARESEDU-2018 [Proc. 7 Int. Conf. MARESEDU-2018]. Tver’: Polipress Publ., 2019, vol. 4, pp. 227–229. (In Russ.).
44. Trefault N., De la Iglesia R., Moreno-Pino M. et al. Annual phytoplankton dynamics in coastal waters from Fildes Bay, Western Antarctic Peninsula. Sci. Rep., 2021, vol. 11, 1368. https://doi.org/10.1038/s41598-020-80568-8
45. Yoshimura S. Abnormal Thermal Stratifications of Inland Lakes. Proc. Imperial Acad., 1937, vol. 13, pp. 316–319. https://doi.org/10.2183/pjab1912.13.316
46. Zhang J., Kobert K., Flouri T., Stamatakis A. PEAR: a fast and accurate Illumina Paired-End reAd merger. Bioinformatics, 2014, vol. 30, no. 5, pp. 614–620. https://doi.org/10.1093/bioinformatics/btt593
Review
For citations:
Plotnikov A.O., Selivanova E.A., Khlopko Yu.A., Voronov D.A., Matorin D.N., Todorenko D.A., Krasnova E.D. Structure and Functioning of Plankton Communities of Phototrophic and Mixotrophic Protists in the Coastal Lagoon “Lake Kislo-Sladkoe” (White Sea, Karelian Coast). Izvestiya Rossiiskoi Akademii Nauk. Seriya Geograficheskaya. 2022;86(6):985–1001. (In Russ.) https://doi.org/10.31857/S2587556622060127