Cite this paper:
Elena D. KRASNOVA, Dmitry N. MATORIN, Tatiana A. BELEVICH, Ludmila E. EFIMOVA, Anastasiia V. KHARCHEVA, Natalia M. KOKRYATSKAYA, Galina N. LOSYUK, Daria A. TODORENKO, Dmitry A. VORONOV, Svetlana V. PATSAEVA. The characteristic pattern of multiple colored layers in coastal stratified lakes in the process of separation from the White Sea[J]. HaiyangYuHuZhao, 2018, 36(6): 1962-1977

The characteristic pattern of multiple colored layers in coastal stratified lakes in the process of separation from the White Sea

Elena D. KRASNOVA1, Dmitry N. MATORIN1, Tatiana A. BELEVICH1, Ludmila E. EFIMOVA2, Anastasiia V. KHARCHEVA3, Natalia M. KOKRYATSKAYA4, Galina N. LOSYUK4, Daria A. TODORENKO1, Dmitry A. VORONOV5,6, Svetlana V. PATSAEVA3
1 Biological Faculty of Lomonosov Moscow State University; Leninskye Gory, 1, bld. 12, Moscow 119234, Russia;
2 Faculty of Geography, Lomonosov Moscow State University; GSP-1, Leninskye Gory, 1, Moscow 119991, Russia;
3 Faculty of Physics, Lomonosov Moscow State University; Leninskye Gory, 1, Moscow 119991, Russia;
4 N. Laverov Federal Center for Integrated Arctic Research, Russian Academy of Sciences; Severnoj Dviny Emb. 23, Arkhangelsk 163000, Russia;
5 A. A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences; Bolshoy Karetny Per. 19, bld. 1, Moscow 127051, Russia;
6 A. N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University; Leninskye Gory, 1, Bld. 40, Moscow 119991, Russia
Abstract:
An unusual feature of the saline stratified lakes that were formed due to ongoing postglacial uplift on the White Sea coast is the presence of several differently colored thin layers in the zone with sharp gradients. Colored layers in five lakes at various stages of separation from the sea were investigated using optical microscopy, spectrophotometry, spectrofluorimetry, and photobiology. The upper greenish colored layer located in the aerobic strata of all lakes near the compensation depth of 1% light penetration contains green algae. In the chemocline, another layer, brightly green, red or pink, is dominated by mixotrophic flagellates. Despite the very low light intensities and the presence of H2S, active photosynthesis by these algae appears to be occurring, as indicated by high values of the maximum quantum yield of primary photochemistry, electron transport activity, photosynthetic activity of photosystem Ⅱ, the fraction of active centers, and low values of heat dissipation. In the reduced zone of the chemocline, a dense green or brown suspension of anoxygenic phototrophs (green sulfur bacteria) is located.
Key words:    algal blooms|coastal lakes|chemocline|fluorescence kinetics|Arctic|White Sea   
Received: 2017-11-10   Revised:
Tools
PDF (896 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Elena D. KRASNOVA
Articles by Dmitry N. MATORIN
Articles by Tatiana A. BELEVICH
Articles by Ludmila E. EFIMOVA
Articles by Anastasiia V. KHARCHEVA
Articles by Natalia M. KOKRYATSKAYA
Articles by Galina N. LOSYUK
Articles by Daria A. TODORENKO
Articles by Dmitry A. VORONOV
Articles by Svetlana V. PATSAEVA
References:
Altenbach A V, Bernhard J M, Seckbach J. 2012. Anoxia:Evidence for Eukaryote Survival and Paleontological Strategies. Springer, Dordrecht. 648p.
Anderson G C. 1969. Subsurface chlorophyll maximum in the northeast Pacific Ocean. Limnol. Oceanogr., 14(3):386-391.
Behnke A, Bunge J, Barger K, Breiner H W, Alla V, Stoeck T. 2006. Microeukaryote community patterns along an O2/H2S gradient in a supersulfidic anoxic fjord (Framvaren, Norway). Appl. Environ. Microbiol., 72(5):3 626-3 636.
Buvalyy S, Garmaeva S, Mardashova M, Krasnova E, Menshenina L. 2015. Macrobenthos composition at the shoreline of Kislo-Sladkoye Lake, separating from the White Sea. EARSeL eProceedings, 14(S1):63-70.
Camacho A. 2006. On the occurrence and ecological features of deep chlorophyll maxima (DCM) in Spanish stratified lakes. Limnetica, 25(1-2):453-478.
Castenholz R W, Utkilen H C. 1984. Loss of sulfide adaptation ability in a thermophilic Oscillatoria. Arch. Microbiol., 138(4):306-309.
Clegg M R, Gaedke U, Boehrer B, Spijkerman E. 2012.Complementary ecophysiological strategies combine to facilitate survival in the hostile conditions of a deep chlorophyll maximum. Oecologia, 169(3):609-622.
Cullen J J. 2015. Subsurface chlorophyll maximum layers:enduring enigma or mystery solved? Annu. Rev. Mar.Sci., 7:207-239.
Dubinin A V, Demidova T P, Kremenetskii V V, Kokryatskaya N M, Rimskaya-Korsakova M N, Yakushev E V. 2012.Determination of the reduced sulfur species in the anoxic zone of the Black Sea:a comparison of the spectrophotometry and iodometry techniques.Oceanology, 52(2):181-190.
Falkowski P G, Raven J A. 2007. Aquatic Photosynthesis.Princeton University Press, Princeton. 488p.
Flynn K J, Davidson K, Cunningham A. 1996. Prey selection and rejection by a microflagellate:implications for the study and operation of microbial food webs. J. Exp. Mar.Biol. Ecol., 196(1-2):357-372.
Gentien P, Reguera B, Yamazaki H, Fernand L, Berdalet E, Raine R. 2008. Global ecology and oceanography of harmful algal blooms. GEOHAB Core Research Project:HABs in Stratified Systems. SCOR and IOC, Baltimore and Paris.
Gervais F. 1998. Ecology of cryptophytes coexisting near a freshwater chemocline. Freshw. Biol., 39(1):61-78.
Gies E A, Konwar K M, Beatty J T, Hallam S J, Löffler F E. 2014. Illuminating microbial dark matter in meromictic Sakinaw Lake. Appl. Environ. Microbiol., 80(21):6 807-6 818.
Gorlenko V M, Vainshtein M B, Kachalkin V I. 1978.Microbiological characteristic of lake Mogilnoye. Arch.Hydrobiol., 81(4):475-492.
Hakala A. 2004. Meromixis as a part of lake evolution-observations and a revised classification of true meromictic lakes in Finland. Boreal Environ. Res, 9:37-53.
Hamilton D P, O'Brien K R, Burford M A, Brookes J D, McBride C G. 2010. Vertical distributions of chlorophyll in deep, warm monomictic lakes. Aquat. Sci., 72(3):295-307.
Hansen F C, Witte H J, Passarge J. 1996. Grazing in the heterotrophic dinoflagellate Oxyrrhis marina:size selectivity and preference for calcified Emiliania huxleyi cells. Aquat. Microb. Ecol., 10(3):307-313.
Hansen P J. 1992. Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale. Mar. Biol., 114(2):327-334.
He G N, Zhang H, King J D, Blankenship R E. 2014. Structural analysis of the homodimeric reaction center complex from the photosynthetic green sulfur bacterium Chlorobaculum tepidum. Biochemistry, 53(30):4 924-4 930.
Hillebrand H, Dürselen C D, Kirschtel D, Zohary T, Pollingher U. 1999. Biovolume calculation for pelagic and benthic microalgae. J. Phycol., 35(2):403-424.
Hutchinson G E. 1937. A contribution to the limnology of arid regions:primarily founded on observations made in the Lahontan Basin. Trans. Connecticut Acad. Arts Sci., 33:47-132.
Il'yash L V, Belevich T A, Matorin D N. 2013. Fluorescence parameters of White Sea phytoplankton under different nitrogen sources. Moscow Univ. Biol. Sci. Bull., 68(1):44-48.
Jeong H J, Seong K A, Yoo D Y, Kim T H, Kang N S, Kim S, Park J Y, Kim J S, Kim G H, Song J Y. 2008. Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria. J. Eukaryot.Microbiol., 55(4):271-288.
John D M, Whitton B A, Brook A J. 2002. The Freshwater Algal Flora of the British Isles:An Identification Guide to Freshwater and Terrestrial Algae. Cambridge University Press, Cambridge. 702p.
Kharcheva A V, Krasnova E D, Voronov D A, Patsaeva S V. 2015. Spectroscopic study of the microbial community in chemocline zones of relic meromictic lakes separating from the White Sea. In:Proceedings of SPIE 9448, Saratov Fall Meeting 2014:Optical Technologies in Biophysics and Medicine XVI; Laser Physics and Photonics XVI; and Computational Biophysics. SPIE, Saratov, Russian Federation, https://doi.org/10.1117/12.2180066.
Kharcheva A V, Zhiltsova A A, Lunina O N, Savvichev A S, Patsaeva S V. 2016. Quantification of two forms of green sulfur bacteria in their natural habitat using bacteriochlorophyll fluorescence spectra. In:Proceedings of SPIE 9917, Saratov Fall Meeting 2015:Third International Symposium on Optics and Biophotonics and Seventh Finnish-Russian Photonics and Laser Symposium(PALS). SPIE, Saratov, Russian Federation, https://doi.org/10.1117/12.2229848.
Kokryatskaya N M, Zabelina S A, Savvichev A S, Morev O Y, Vorobjeva T Y. 2012. Seasonal biogeochemical and microbiological studies of small lakes in taiga zone of Northwestern Russian (Arkhangelsk Province). Water Resour., 39(1):105-117.
Kondo R, Nakagawa A, Mochizuki L, Osawa K, Fujioka Y, Butani J. 2009. Dominant bacterioplankton populations in the meromictic Lake Suigetsu as determined by denaturing gradient gel electrophoresis of 16S rRNA gene fragments.Limnology, 10(1):63-69.
Krasnova E D, Kharcheva A V, Milyutina I A, Voronov D A, Patsaeva S V. 2015a. Study of microbial communities in redox zone of meromictic lakes isolated from the White Sea using spectral and molecular methods. J. Mar. Biol.Assoc. UK, 95(8):1 579-1 590.
Krasnova E D, Pantyulin A N, Belevich T A, Voronov D A, Demidenko N A, Zhitina L S, Ilyash L V, Kokryatskaya N M, Lunina O N, Mardashova M V, Prudkovsky A A, Savvichev A S, Filippov A S, Shevchenko V P. 2013.Multidisciplinary studies of the separating lakes at different stage of isolation from the White Sea performed in March 2012. Oceanology, 53(5):639-642.
Krasnova E D, Pantyulin A N, Matorin D N, Todorenko D A, Belevich T A, Milyutina I A, Voronov D A. 2014.Cryptomonad alga Rhodomonas sp. (Cryptophyta, Pyrenomonadaceae) bloom in the redox zone of the basins separating from the White Sea. Microbiology, 83(3):270-277.
Krasnova E, Voronov D, Frolova N, Pantyulin A, Samsonov T. 2015b. Salt lakes separated from the White Sea. EARSeL eProceedings, 14(S1):8-22.
Lauro F M, DeMaere M Z, Yau S, Brown M V, Ng C, Wilkins D, Raftery M J, Gibson J A, Andrews-Pfannkoch C, Lewis M, Hoffman J M, Thomas T, Cavicchioli R. 2011. An integrative study of a meromictic lake ecosystem in Antarctica. ISME J., 5(5):879-895.
Laybourn-Parry J, Marshall W A. 2003. Photosynthesis, mixotrophy and microbial plankton dynamics in two high Arctic lakes during summer. Polar Biol., 26(8):517-524.
Laybourn-Parry J, Roberts E C, Bell E M. 2000. Mixotrophy as a survival strategy in Antarctic lakes. In:Davidson W, Howard-Williams C, Broady P eds. Antarctic Ecosystems:Models for Wider Ecological Understanding. The Caxton Press, Christchurch. p.33-40.
Laybourn-Parry J. 2002. Survival mechanisms in Antarctic lakes. Philos. Trans. Roy. Soc. Biol. Sic., 357(1423):863-869.
Ludlam S D. 1996. The comparative limnology of high arctic, coastal, meromictic lakes. J. Paleolimnol., 16(2):111-131.
Lunina O N, Savvichev A S, Krasnova E D, Kokryatskaya N M, Veslopolova E F, Kuznetsov B B, Gorlenko V M. 2016.Succession processes in the anoxygenic phototrophic bacterial community in lake Kislo-Sladkoe (Kandalaksha bay, White Sea). Microbiology, 85(5):570-582.
Matorin D N, Antal T K, Ostrowska M, Rubin A B, Ficek D, Majchrowski R. 2004. Chlorophyll fluorimetry as a method for studying light absorption by photosynthetic pigments in marine algae. Oceanologia, 46(4):519-531.
Matorin D N, Todorenko D A, Seifullina N K, Zayadan B K, Rubin A B. 2013. Effect of silver nanoparticles on the parameters of chlorophyll fluorescence and P700 reaction in the green alga Chlamydomonas reinhardtii.Microbiology, 82(6):809-814.
Menden-Deuer S, Lessard E J. 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr., 45(3):569-579.
Moiseenko T I, Gashkina N A. 2010. Formirovanie Khimicheskogo Sostava Vod Ozer v Usloviyakh Izmeneniya Okruzhayushchey Sredy[The Formation of the Chemical Composition of Lakes Water in a Changing Environment]. Nauka, Moscow. (in Russian)
Mori Y, Kataoka T, Okamura T, 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. Arch. Microbiol., 195(5):303-312.
Nakajima Y, Shimizu H, Ogawa N O, Sakamoto T, Okada H, Koba K, Kitazato H, Ohkouchi N. 2004. Vertical distributions of stable isotopic compositions and bacteriochlorophyll homologues in suspended particulate matter in saline meromictic Lake Abashiri. Limnology, 5(3):185-189.
Neklyudov I M, Borts B V, Polevich O V, Tkachenko V I, Shilyaev B A. 2006. An alternative hydrogen sulfide energy of Black sea. The state, problems and perspectives.Int. Sci. J. Altern. Energy Ecol. Ecology (Sarov, Russ.Fed.), 12(44):23-30.
Okada M, Taniuchi Y, Murakami A, Takaichi S, Ohtake S, Ohki K. 2007. Abundance of picophytoplankton in the halocline of a meromictic lake, Lake Suigetsu, Japan.Limnology, 8(3):271-280.
Oren A, Padan E, Malkin S. 1979. Sulfide inhibition of photosystem Ⅱ in cyanobacteria (blue-green algae) and tobacco chloroplasts. Biochim. Biophys. Acta, 546(2):270-279.
Orf G S, Blankenship R E. 2013. Chlorosome antenna complexes from green photosynthetic bacteria.Photosynth. Res., 116(2-3):315-331.
Overmann J, Beatty J T, Hall K J, Pfennig N, Northcote T G. 1991. Characterization of a dense, purple sulfur bacterial layer in a meromictic salt lake. Limnol. Oceanogr., 36(5):846-859.
Overmann J, Garcia-Pichel F. 2000. The phototrophic way of life. In:Rosenberg E, DeLong E F, Lory S, Stackebrand E, Thompson F eds. The Prokaryotes:Prokaryotic Communities and Ecophysiology. Springer, New York.p.203-257.
Pancaldi S, Baldisserotto C, Ferroni L, Bonora A, Fasulo M P. 2002. Room temperature microspectrofluorimetry as a useful tool for studying the assembly of the PSⅡ chlorophyll-protein complexes in single living cells of etiolated Euglena gracilis Klebs during the greening process. J. Exp. Bot., 53(375):1 753-1 763.
Rogozin D Y, Trusova M Y, Khromechek E B, Degermendzhy A G. 2010. Microbial community of the chemocline of the meromictic lake Shunet (Khakassia, Russia) during summer stratification. Microbiology, 79(2):253-261.
Sapozhnikov V V. 2003. Rukovodstvo po khimicheskomu analizu morskikh i presnykh vod pri ekologicheskom monitoringe rybokhozyaistvennykh vodoemov i perspektivnykh dlya promysla raionov Mirovogo okeana(Guide on Chemical Analysis of Sea and Fresh Water in the Environmental Monitoring of Water Bodies Used for Fishery and Commercially Promising Regions of the World Ocean). VNIRO, Moscow. 202p. (in Russian)
Shaporenko S I, Koreneva G A, Pantyulin A N, Pertsova N M. 2005. Characteristics of the ecosystems of water bodies separating from Kandalaksha Bay of the White Sea. Water Resour., 32(5):469-483.
Simmonds B, Wood S A, Özkundakci D, Hamilton D P. 2015.Phytoplankton succession and the formation of a deep chlorophyll maximum in a hypertrophic volcanic lake.Hydrobiologia, 745(1):297-312.
Strasser R J, Tsimilli-Michael M, Srivastava A. 2004. Analysis of the chlorophyll a fluorescence transient. In:Papageorgiou G C, Govindjee eds. Chlorophyll a Fluorescence:a signature of Photosynthesis. Springer, Dordrecht. p.321-362.
Strelkov P, Shunatova N, Fokin M, Usov N, Fedyuk M, Malavenda S, Lubina O, Poloskin A, Korsun S. 2014. Marine Lake Mogilnoe (Kildin Island, the Barents Sea):one hundred years of solitude. Polar Biol., 37(3):297-310.
Subetto D A, Shevchenko V P, Ludikova A V, Kuznetsov D D, Sapelko T V, Lisitsyn A P, Evzerov V Y, Van Beek P, Souhaut M, Subetto G D. 2012. Chronology of isolation of the Solovetskii Archipelago lakes and current rates of lake sedimentation. Dokl. Earth Sci., 446(1):1 042-1 048.
Tonolla M, Peduzzi S, Demarta A, Peduzzi R, Hahn D. 2004.Phototropic sulfur and sulfate-reducing bacteria in the chemocline of meromictic Lake Cadagno, Switzerland. J.Limnol., 63(2):161-170.
Van Der Weij-De Wit C D, Doust A B, Van Stokkum I H M, Dekker J P, Wilk K E, Curmi P M G, Scholes G D, Van Grondelle R. 2006. How energy funnels from the phycoerythrin antenna complex to photosystem I and photosystem Ⅱ in cryptophyte Rhodomonas CS24 cells. J.Phys. Chem. B, 110(49):25 066-25 073.
Van Hove P, Belzile C, Gibson J A, Vincent W F. 2006. Coupled landscape-lake evolution in High Arctic Canada. Can. J.Earth Sci., 43(5):533-546.
Vincent W F, Laybourn-Parry J. 2008. Polar Lakes and Rivers:Limnology of Arctic and Antarctic Aquatic Ecosystems.Oxford University Press, Oxford. 346p.
Weller D, Doemel W, Brock T D. 1975. Requirement of low oxidation-reduction potential for photosynthesis in a bluegreen alga (Phormidium sp.). Arch. Microbiol., 104(1):7-13.