Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-22T06:29:14.289Z Has data issue: false hasContentIssue false
  • English
  • Français

Study of microbial communities in redox zone of meromictic lakes isolated from the White Sea using spectral and molecular methods

Published online by Cambridge University Press:  01 July 2015

E.D. Krasnova ,
A.V. Kharcheva ,
I.A. Milyutina ,
D.A. Voronov  and
S.V. Patsaeva Open the ORCID record for S.V. Patsaeva [Opens in a new window]
E.D. Krasnova*
Affiliation:
Biological Faculty of Lomonosov Moscow State University, Leninskye gory, 1, bld. 12, 119234 Moscow, Russia
A.V. Kharcheva
Affiliation:
Faculty of Physics, Lomonosov Moscow State University, Leninskye gory, 1, bld. 2, Moscow 119991, Russia
I.A. Milyutina
Affiliation:
A.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Leninskye gory, 1, bld. 40, Moscow 119992, Russia
D.A. Voronov
Affiliation:
A.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Leninskye gory, 1, bld. 40, Moscow 119992, Russia A.A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Bolshoy Karetny per. 19, Moscow 127994, Russia
S.V. Patsaeva
Affiliation:
Faculty of Physics, Lomonosov Moscow State University, Leninskye gory, 1, bld. 2, Moscow 119991, Russia
*
Correspondence should be addressed to: E.D. Krasnova, Leninskye gory, 1, bld. K, apt. 131, Moscow, 119234, Russia email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Due to postglacial isostatic uplift many stratified lakes, at different stages of isolation, are located along the shores of the White Sea. In five lakes, located near the White Sea Biological Station of Moscow State University, salinity, temperature, pH, concentration of dissolved oxygen, redox potential, and illuminance were measured. Distribution of microorganisms and spectral properties of water layers were also studied. All the lakes had a narrow bright coloured layer in the redox zone caused by mass development of phototropic microorganisms. Light absorption and fluorescence spectra indicated algae containing chlorophyll a predominate in the red water layers while the colouration of green and brown layers is caused by green sulphur bacteria with bacteriochlorophylls d and e. Sunlight is completely absorbed in the redox zone because of the high density of algae and/or bacteria, resulting in aphotic conditions below. Coloured layers act as a specific biotope for special communities of microorganisms. Eukaryotes identified by the 18S rRNA gene included different species of mixotrophic algae and ciliates resistant to anoxia. The water layer colour and spectral characteristics (i.e. light absorption and fluorescence) of water in the redox zone can be considered indicators of the stage of lake isolation from the sea, with the red colour caused by cryptophyte alga Rhodomonas sp. bloom found in earlier stages and brown and green colours caused by green sulphur bacteria in later stages.

Keywords

Meromictic lakechemoclineredox zoneabsorption and fluorescence spectrachlorophyllbacteriochlorophyllmicrobial communityWhite Sea
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 8 , December 2015 , pp. 1579 - 1590
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Altenbach, A.V., Bernhard, J.M. and Seckbach, J. (eds) (2012) Anoxia: evidence for eukaryote survival and paleontological strategies. Dordrecht: Springer.CrossRefGoogle Scholar
Anderson, G.C. (1958) Some limnological features of a shallow saline meromictic lake. Limnology and Oceanography 3, 259–270.CrossRefGoogle Scholar
Antal, T.K., Venediktov, P.S., Matorin, D.N., Ostrowska, M., Woźniak, B. and Rubin, A.B. (2001) Measurement of phytoplankton photosynthesis rate using a pump-and-probe fluorometer. Oceanologia 43, 291–313.Google Scholar
Behnke, A., Bunge, J., Barger, K., Breiner, H.-W., Alla, V. and Stoeck, Th. (2006) Microeukaryote community patterns along an O2/H2S gradient in a supersulfidic anoxic fjord (Framvaren, Norway). Applied and Environmental Microbiology 72, 3626–3636.CrossRefGoogle Scholar
Burton, H.R. (1981) Chemistry, physics and evolution of Antarctic saline lakes. Developments in Hydrobiology 5, 339–362.CrossRefGoogle Scholar
Dugan, H.A. and Lamoureux, S.F. (2011) The chemical development of a hypersaline coastal basin in the High Arctic. Limnology and Oceanography 56, 495–507.CrossRefGoogle Scholar
Fenchel, T. and Finaly, B.J. (1990) Anaerobic free-living protozoa: growth efficiencies and the structure of anaerobic communities. FEMS Microbiology Letters 74, 269–275.CrossRefGoogle Scholar
Fenchel, T., Perry, T. and Thane, A. (1977) Anaerobiosis and symbiosis with bacteria in free-living ciliates. Journal of Protozoology 24, 154–163.CrossRefGoogle ScholarPubMed
Gibson, J.E. (1999). The meromictic lakes and stratified marine basins of the Vestfold Hills, East Antarctica. Antarctic Science 11, 175–192.CrossRefGoogle Scholar
Gorlenko, V.M., Vainstein, M.B. and Kachalkin, V.I. (1978) Microbiological characteristic of lake Mogilnoye. Archiv fur Hydrobiologie 81, 475–492.Google Scholar
Gorshkova, O.M., Milukov, A.S., Patsayeva, S.V. and Yuzhakov, V.I. (2006) Fluorescence of DOM nanoparticles in natural water. Proceedings of SPIE, Atomic and Molecular Pulsed Lasers VI 6263, 248–255.Google Scholar
Hakala, A. (2004) Meromixis as a part of lake evolution – observations and a revised classification of true meromictic lakes in Finland. Boreal Environment Research 9, 37–53.Google Scholar
Hammer, A.C. and Pitchford, J.W. (2005) The role of mixotrophy in plankton bloom dynamics, and the consequences for productivity. ICES Journal of Marine Science 62, 833–840.CrossRefGoogle Scholar
Jones, R.I. (2000) Mixotrophy in planktonic protists: an overview. Freshwater Biology 45, 219–226.CrossRefGoogle Scholar
Kharcheva, A.V., Meschankin, A.V., Lyalin, I.I., Krasnova, E.D., Voronov, D.A. and Patsaeva, S.V. (2014) The study of coastal meromictic water basins in the Kandalaksha Gulf of the White Sea by spectral and physicochemical methods. Proceedings SPIE, 9031, Saratov Fall Meeting 2013: Optical Technologies in Biophysics and Medicine XV; and Laser Physics and Photonics XV, 90310T (January 30, 2014); doi: 10.1117/12.2051737.CrossRefGoogle Scholar
Kokryatskaya, N., Krasnova, E. and Losyuk, G. (2014) Features of formation of hydrogen sulphide contamination in the separating lakes in the Kandalaksha bay of the White Sea. In Tzetlin, A., Reuter, R., Patsaeva, S., Krasnova, E. and Dolenko, T. (eds) Abstracts of lectures and poster presentations of the International White Sea Student Workshop on Optics of Coastal Waters; Nikolai Pertsov White Sea Biological Station of Lomonosov Moscow State University; Republic of Karelia, Russia, 30 August – 7 September, 2014. — WSBS – Moscow, 2014, 17–18.Google Scholar
Korde, N.V. (1956) The methods of biological studies for the bottom deposits of lakes (the field methods of biological analysis). In Pavlovsky, E.N. and Zhadin, V.I. (eds) Life in fresh waters of USSR. Moscow: Nauka Press, pp. 383–413. [In Russian]Google Scholar
Krasnova, E.D., Pantyulin, A.N., Belevich, T.A., Voronov, D.A., Demidenko, N.A., ZhitinaL, S., Ilyash, L.V., Kokryatskaya, N.M., Lunina, O.N., Mardashova, M.V., Prudkovsky, A.A., Savvichev, A.S., Filippov, A.S. and Shevchenko, V.P. (2013a) Multidisciplinary studies of the separating lakes at different stage of isolation from the White Sea performed in March 2012. Oceanology 53, 639–642.CrossRefGoogle Scholar
Krasnova, E.D., Pantyulin, A.N., Matorin, D.N., Todorenko, D.A., Belevich, T.A., Milyutina, I.A. and Voronov, D.A. (2014) Blooming of the cryptomonad alga Rhodomonas sp. (Cryptophyta, Pyrenomonadaceae) in the redox zone of the basins separating from the White Sea. Microbiology (Microbiologia) 83, 270–277.Google ScholarPubMed
Krasnova, E.D., Voronov, D.A. and Voronova, A.D. (2013b) The role of sea ice brine for the formation of vertical stratification in reservoirs separating from the White Sea (in Rus., Eng. abstract). In Geology of the Seas and Oceans: Proceedings of XX International Scientific Conference (School) on Marine Geology, III. Moscow: GEOS, pp. 201–205.Google Scholar
Losyuk, G., Kokryatskaya, N. and Krasnova, E. (2014) Distribution of hydrogen sulfide in the lake Trekhtsvetnoe and the lagoon (lake) on the Zelenyi Cape. In Tzetlin, A., Reuter, R., Patsaeva, S., Krasnova, E. and Dolenko, T. (eds) Abstracts of lectures and poster presentations of the International White Sea Student Workshop on Optics of Coastal Waters; Nikolai Pertsov White Sea Biological Station of Lomonosov Moscow State University; Republic of Karelia, Russia, 30 August – 7 September, 2014. – WSBS – Moscow, 2014, 21–22.Google Scholar
Ludlam, S.D. (1996) The comparative limnology of high arctic, coastal, meromictic lakes. Journal of Paleolimnology 16, 111–131.CrossRefGoogle Scholar
Lunina, O.N., Savvichev, A.S., Kuznetsov, B.B., Pimenov, N.V. and Gorlenko, V.M. (2013) Anoxygenic phototrophic bacteria of the Kislo-Sladkoe stratified lake (White Sea, Kandalaksha Bay). Microbiology (Microbiologia) 82, 815–832.Google Scholar
Lynn, D.H. and Strüder-Kypke, M. (2002) Phylogenetic position of Licnophora, Lechriopyla, and Schizocaryum, three unusual ciliates (phylum Ciliophora) endosymbiotic in echinoderms (phylum Echinodermata). Journal of Eukaryotic Microbiology 49, 460–468.CrossRefGoogle ScholarPubMed
Medlin, L., Elwood, H.J., Stickel, S. and Sogin, M.L. (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71, 491–499.CrossRefGoogle ScholarPubMed
Millero, F.J. (1991) The oxidation of H2S in Framvaren Fjord. Limnology and Oceanography 36, 1007–1014.CrossRefGoogle Scholar
Mori, Y., Kataoka, T., Okamura, T. and Kondo, R. (2013) Dominance of green sulfur bacteria in the chemocline of the meromictic Lake Suigetsu, Japan, as revealed by dissimilatory sulfite reductase gene analysis. Archives of Microbiology 195, 303–312.CrossRefGoogle ScholarPubMed
Nekludov, I.M., Bortz, B.V., Polevich, O.V., Tkacjenko, V.I. and Shilyaev, B.A. (2006) Alternative hydrogen sulfide energy in the Black Sea. Status, problems and prospects. Alternative Energy and Ecology 12, 23–30. [In Russian]Google Scholar
Oikonomou, A., Katsiapi, M., Karayanni, H., Moustaka-Gouni, M. and Kormas, K.A. (2012) Plankton microorganisms coinciding with two consecutive mass fish kills in a newly reconstructed lake. Scientific World Journal, 504135. doi: 10.1100/2012/504135.Google Scholar
Ouellet, M., Dickman, M., Bisson, M. and Pagé, P. (1989) Physico-chemical characteristics and origin of hypersaline meromictic Lake Garrow in the Canadian High Arctic. Hydrobiologia 172, 215–234.CrossRefGoogle Scholar
Overmann, J., Beatty, J.T., Hall, K.J., Pfennig, N. and Northcote, T.G. (1991) Characterization of dense, purple sulfur bacterial layer in meromictic salt lake. Limnology and Oceanography 36, 846–859.CrossRefGoogle Scholar
Patsayeva, S. and Reuter, R. (1995) Spectroscopic study of major components of dissolved organic matter naturally occurring in water. Proceedings of SPIE, 2586, Global Process Monitoring and Remote Sensing of the Ocean and Sea Ice (December 18, 1995) , pp. 151–160.CrossRefGoogle Scholar
Roberts, E.C. and Laybourn-Parry, J. (1999) Mixotrophic cryptophytes and their predators in the Dry Valley lakes of Antarctica. Freshwater Biology 41, 737–746.CrossRefGoogle Scholar
Rogozin, D.Y., Trusova, M.Y., Khromechek, E.B., and Degermendzhy, A.G. (2010) Microbial community of the chemocline of the meromictic lake Shunet (Khakassia, Russia) during summer stratification. Microbiology (Mikrobiologiya) 79, 253–261.Google Scholar
Romanenko, F.A. and Shilova, O.S. (2012) The postglacial uplift of the Karelian coast of the White Sea according to radiocarbon and diatom analyses of lacustrine-boggy deposits of Kindo peninsula. Doklady Earth Sciences 442, 242–246.CrossRefGoogle Scholar
Savvichev, A.S., Lunina, O.N., Rusanov, I.I., Zakharova, E.E., Veslopolova, E.F. and Ivanov, M.V. (2014) Microbiological and isotopic geochemical investigation of Lake Kislo-Sladkoe, a meromictic water body at the Kandalaksha Bay shore (White Sea). Microbiology (Microbiologia) 83, 56–66.Google ScholarPubMed
Savvichev, A.S., Rusanov, I.I., Zakharova, E.E., Lunina, O.N., Bryantseva, I.A., Yusupov, S.K., Pimenov, N.V., Ivanov, M.V., Rogozin, D.Yu. and Degermendzhi, A.G. (2005) Microbiological and isotopic-geochemical investigations of meromictic lakes in Khakasia in winter. Microbiology (Mikrobiologiya) 74, 477–485.Google ScholarPubMed
Schwarz, M.V.J., Zuendorf, A. and Stoeck, T. (2007) Morphology, ultrastructure, molecular phylogeny, and autecology of Euplotes elegans Kahl, 1932 (Hypotrichida; Euplotidae) isolated from the anoxic Mariager Fjord, Denmark. Journal of Eukaryotic Microbiology 54, 125–136.CrossRefGoogle Scholar
Shaporenko, S.I., Koreneva, G.A., Pantyulin, A.N. and Pertsova, N.M. (2005) Characteristics of the ecosystems of water bodies separating from Kandalaksha bay of the White Sea. Water Resources 32, 469–483.CrossRefGoogle Scholar
Shubina, D.M., Patsaeva, S.V., Yuzhakov, V.I., Gorshkova, O.M. and Fedoseeva, E.V. (2009) Fluorescence of organic matter dissolved in natural water. Water: Chemistry and Ecology 11, 31–37. http://watchemec.ru/en/article/12980/.Google Scholar
Storelli, N., Peduzzi, S., Saad, M., Frigaard, N.-U., Perret, X. and Tonolla, M. (2013) CO2 assimilation in the chemocline of Lake Cadagno is dominated by a few types of phototrophic purple sulfur bacteria. FEMS Microbiology Ecology 86, 421–432.CrossRefGoogle Scholar
Strelkov, P., Shunatova, N., Fokin, M., Usov, N., Fedyuk, M., Malavenda, S., Lubina, O., Poloskin, A. and Korsun, S. (2014) Marine Lake Mogilnoe (Kildin Island, the Barents Sea): one hundred years of solitude. Polar Biology 37, 297–310.CrossRefGoogle Scholar
Subetto, D.A., Shevchenko, V.P., Lisitsyn, A.P., Ludikova, A.V., Kuznetsov, D.D., Sapelko, T.V., Evzerov, V.Ya., Van Beek, P., Souhaut, M. and Subetto, G.D. (2012) Chronology of isolation of the Solovetskii archipelago lakes and current rates of lake sedimentation. Doklady Earth Sciences 446, 1042–1048.CrossRefGoogle Scholar
Tonolla, M., Peduzzi, S., Demarta, A., Peduzzi, R. and Hahn, D. (2004) Phototropic sulfur and sulfate-reducing bacteria in the chemocline of meromictic Lake Cadagno, Switzerland. Journal of Limnology 63, 161–170.CrossRefGoogle Scholar
Williams, W.D. (1996) The largest, highest and lowest lakes of the world: saline lakes. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 26, 61–79.Google Scholar
Zenkevitsch, L.A. (1928) Zur Charakteristik der salzhaltigen Uferseen der Sudinsel von Nowaja Zemlja. Russische Hydrobiologische Zeitschrift 7, 183–187.Google Scholar