Skip to main content
SpringerLink
Log in

Effect of salinity on diazotrophic activity and microbial composition of phototrophic communities from Bitter-1 soda lake (Kulunda Steppe, Russia)

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

Bitter-1 is a shallow hypersaline soda lake in Kulunda Steppe (Altai region, Russia). During a study period between 2005 and 2016, the salinity in the littoral area of the lake fluctuated within the range from 85 to 400 g/L (in July of each year). Light-dependent nitrogen fixation occurred in this lake up to the salt-saturating conditions. The rates increased with a decrease in salinity, both under environmental conditions and in laboratory simulations. The salinities below 100 g/L were favorable for light-dependent nitrogen fixation, while the process was dramatically inhibited above 200 g/L salts. The analysis of nifH genes in environmental samples and in enrichment cultures of diazotrophic phototrophs suggested that anaerobic fermenting and sulfate-reducing bacteria could participate in the dark nitrogen fixation process up to soda-saturating conditions. However, we cannot exclude the possibility that haloalkaliphilic nonheterocystous cyanobacteria (Euhalothece sp. and Geitlerinema sp.) and anoxygenic purple sulfur bacteria (Ectothiorhodospira sp.) might also play a role in the process at light conditions. The heterocystous cyanobacterium Nodularia sp. develops at low salinity (below 80 g/L) that is not characteristic for Bitter-1 Lake and thus does not make a significant contribution to the nitrogen fixation in this lake.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Axler RP, Gersberg RM, Paulson LJ (1978) Primary productivity in meromictic Big Soda Lake, Nevada. Great Basin Nat 38:187–192

    CAS  Google Scholar 

  • Berman-Frank I, Lundgren P, Falkowski P (2003) Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res Microbiol 154:157–164

    Article  PubMed  CAS  Google Scholar 

  • Bolhuis H, Severin I, Confurius-Guns V, Wollenzien UIA, Stal LJ (2010) Horizontal transfer of the nitrogen fixation gene cluster in the cyanobacterium Microcoleus chthonoplastes. ISME J 4:121–130

    Article  PubMed  CAS  Google Scholar 

  • Boltyanskaya YV, Kevbrin VV, Lysenko AM, Tourova TP, Zhilina TN, Kolganova TV, Osipov GA (2007) Halomonas mongoliensis sp. nov. and Halomonas kenyensis sp. nov., new haloalkaliphilic denitrifiers capable of N2O reduction, isolated from soda lakes. Microbiology (Mikrobiologiya) 76:739–747

    Article  CAS  Google Scholar 

  • Bryantseva IA, Tourova TP, Kostrikina NA, Gorlenko VM, Kovaleva OL (2010) Ectothiorhodospira magna sp. nov., a new large alkaliphilic purple sulfur bacterium. Microbiology (Mikrobiologiya) 79:780–790

    Article  CAS  Google Scholar 

  • Edwards U, Rogall T, Bloeker H, Ende MD, Boeettger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Nucleic Acids Res 17:7843–7853

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Foti MJ, Sorokin DY, Lomans B, Mussman M, Zacharova EE, Pimenov NV, Kuenen JG, Muyzer G (2007) Diversity, activity, and abundance of sulfate-reducing bacteria in saline and hypersaline soda lakes. Appl Environ Microbiol 73:2093–2100

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Foti MJ, Sorokin DY, Zacharova EE, Pimenov NV, Kuenen JG, Muyzer G (2008) Bacterial diversity and activity along a salinity gradient in soda lakes of the Kulunda Steppe (Altai, Russia). Extremophiles 12:133–145

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Pichel F, Nübel U, Muyzer G (1998) The phylogeny of unicellular, extremely halotolerant cyanobacteria. Arch Microbiol 169:469–482

    Article  PubMed  CAS  Google Scholar 

  • Gerasimenko LM, Dubinin AV, Mityushina LL, Zavarzin GA (1999) A microscopic green alga from soda lakes. Microbiology (Mikrobiologiya) 68:610–614

    CAS  Google Scholar 

  • Grant WD (2006) Alkaline environments and biodiversity. In: Gerday C, Glansdorff N (eds) Extremophiles, in Encyclopedia of Life Support Systems (EOLSS), Developed under the Auspices of the UNESCO. Eolss Publishers, Oxford. http://www.eolss.net. Accessed 15 Feb 2018

  • Hardy RW, Holsten R, Jackson E, Burns R (1968) The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Herbert RA (1975) Heterotrophic nitrogen fixation in shallow estuarine sediments. J Exp Mar Biol Ecol 18:215–225

    Article  CAS  Google Scholar 

  • Herbst DB (1998) Potential salinity limitations on nitrogen fixation in sediments from Mono Lake, California. Int J Salt Lake Res 7:261–274

    Google Scholar 

  • Isachenko BL (1934) Chloride, sulfate, and soda lakes of Kulunda Steppe. In: Kulundinskaya ekspeditsiya Akademii nauk SSSR 1931–1933 gg. (Kulunda Expedition of the USSR Academy of Sciences, 1931–1933). 1 (in Russian)

  • Jellison R, Miller LG, Melack JM, Dana GL (1993) Meromixis in hypersaline Mono Lake, California. 2. Nitrogen fluxes. Limnol Oceanogr 38:1020–1039

    Article  CAS  Google Scholar 

  • Kompantseva EI, Komova AV, Sorokin DY (2010) Communities of anoxygenic phototrophic bacteria in the saline soda lakes of the Kulunda Steppe (Altai Krai). Microbiology (Mikrobiologiya) 79:89–95

    Article  CAS  Google Scholar 

  • Krienitz L, Schagerl M (2016) Tiny and tough: microphytes of East African soda lakes. In: Schagerl M (ed) Soda Lakes of East Africa. Springer International Publishing, Switzerland, pp 149–177

    Google Scholar 

  • Marusina AI, Boulygina ES, Kuznetsov BB, Tourova TP, Kravchenko IK, Gal’chenko VF (2001) A system of oligonucleotide primers for the amplification of nifH genes of different taxonomic groups of prokaryotes. Microbiology (Mikrobiologiya) 70:73–78

    Article  CAS  Google Scholar 

  • Medová H, Boldareva EN, Hrouzek P, Borzenko SV, Namsaraev ZB, Gorlenko VM, Namsaraev BB, Koblížek M (2011) High abundances of aerobic anoxygenic phototrophs in saline steppe lakes. FEMS Microbiol Ecol 76:393–400

    Article  PubMed  CAS  Google Scholar 

  • Melack JM (1981) Photosynthetic activity of phytoplankton in tropical African Soda lakes. Hydrobiologia 81:71–85

    Article  Google Scholar 

  • Mikhodyuk OS, Gerasimenko LM, Akimov VN, Ivanovsky RN, Zavarzin GA (2008) Ecophysiology and polymorphism of the unicellular extremely natronophilic cyanobacterium Euhalothece sp. Z-M001 from Lake Magadi. Microbiology (Mikrobiologiya) 77:717–725

    Article  CAS  Google Scholar 

  • Namsaraev ZB (2009) Application of extinction coefficients for quantification of chlorophylls and bacteriochlorophylls. Microbiology (Mikrobiologiya) 78:794–797

    Article  CAS  Google Scholar 

  • Namsaraev ZB, Zaitseva SV, Gorlenko VM, Kozyreva LP, Namsaraev BB (2015) Microbial processes and factors controlling their activities in alkaline lakes of the Mongolian plateau. Chin J Oceanol Limnol 33:1391–1401

    Article  CAS  Google Scholar 

  • Oremland RS (1983) Hydrogen metabolism by decomposing cyanobacterial aggregates in Big Soda Lake, Nevada. Appl Environ Microbiol 45:1519–1525

    PubMed  PubMed Central  CAS  Google Scholar 

  • Oremland RS (1990) Nitrogen fixation dynamics of two diazotrophic communities in Mono Lake, California. Appl Environ Microbiol 56:614–622

    PubMed  PubMed Central  CAS  Google Scholar 

  • Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348

    PubMed  PubMed Central  CAS  Google Scholar 

  • Oren A (2011a) Diversity of halophiles. In: Horikoshi K (ed) Extremophiles handbook. Springer, Japan, pp 309–325

    Chapter  Google Scholar 

  • Oren A (2011b) Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol 13:1908–1923

    Article  PubMed  CAS  Google Scholar 

  • Reznikov AA, Mulikovskaya EP, Sokolov IY (1970) Methods for natural water analysis. Nedra, Moscow, p 118 (in Russian)

    Google Scholar 

  • Rippka R (1988) Isolation and purification of cyanobacteria. Meth Enzymol 167:3–27

    Article  PubMed  CAS  Google Scholar 

  • Samylina OS, Sapozhnikov FV, Gainanova OY, Ryabova AV, Nikitin MA, Sorokin DY (2014) Algo-bacterial communities of the Kulunda Steppe (Altai Region, Russia) soda lakes. Microbiology (Mikrobiologiya) 83:849–860

    Article  CAS  Google Scholar 

  • Schultze-Lam S, Ferris FG, Sherwood-Lollar B, Gerits JP (1996) Ultrastructure and seasonal growth patterns of microbial mats in a temperate climate saline-alkaline lake: Goodenough lake, British Columbia, Canada. Can J Microbiol 42:147–161

    Article  CAS  Google Scholar 

  • Shapovalova AA, Khijniak TV, Tourova TP, Muyzer G, Sorokin DY (2008) Heterotrophic denitrification at extremely high salt and pH by haloalkaliphilic Gammaproteobacteria from hypersaline soda lakes. Extremophiles 12:619–625

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sorokin DY (2017) Anaerobic haloalkaliphiles. In: Encyclopedia of Life Sciences. Wiley, Chichester. https://doi.org/10.1002/9780470015902.a0027654

  • Sorokin DY, Kuenen JG (2005) Alkaliphilic chemolithotrophs from soda lakes. FEMS Microbiol Ecol 52:287–295

    Article  PubMed  CAS  Google Scholar 

  • Sorokin DY, Tourova TP, Henstra AM, Stams AJM, Galinski EA, Muyzer G (2008a) Sulfidogenesis at extremely haloalkaline conditions by Desulfonatronospira thiodismutans gen. nov., sp. nov., and Desulfonatronospira delicata sp. nov.—a novel lineage of Deltaproteobacteria from hypersaline soda lakes. Microbiology (SGM) 154:1444–1453

    Article  CAS  Google Scholar 

  • Sorokin ID, Zadorina EV, Kravchenko IK, Boulygina ES, Tourova TP, Sorokin DY (2008b) Natronobacillus azotifigens gen. nov., sp. nov., an anaerobic diazotrophic haloalkaliphile from soda-rich habitats. Extremophiles 12:819–827

    Article  PubMed  CAS  Google Scholar 

  • Sorokin DY, Abbas B, Tourova TP, Bumazhkin BK, Kolganova TV, Muyzer G (2014a) Sulfate-dependent acetate oxidation under extremely natron-alkaline conditions by syntrophic associations from hypersaline soda lakes. Microbiology (SGM) 160:723–732

    Article  CAS  Google Scholar 

  • Sorokin DY, Berben T, Melton ED, Overmars L, Vavourakis S, Mauzer G (2014b) Microbial diversity and biogeochemical cycling in soda lakes. Extremophiles 18:791–809

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sorokin DY, Banciu HA, Muyzer G (2015a) Functional microbiology of soda lakes. Curr Opin Microbiol 25:88–96

    Article  PubMed  CAS  Google Scholar 

  • Sorokin DY, Chernyh NA, Poroshina MN (2015b) Desulfonatronobacter acetoxydans sp. nov.: a first acetate-oxidizing, extremely salt-tolerant alkaliphilic SRB from a hypersaline soda lake. Extremophiles 19:899–907

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Spiridonova EM, Berg IA, Kolganova TV, Ivanovskii RN, Kuznetsov BB, Tourova TP (2004) An oligonucleotide primer system for amplification of the ribulose-1,5-bisphosphate carboxylase/oxygenase genes of bacteria of various taxonomic groups. Microbiology (Mikrobiologiya) 73:316–325

    Article  CAS  Google Scholar 

  • Tourova TP, Kovaleva OL, Sorokin DY, Muyzer G (2010) Ribulose-1,5-bisphosphate carboxylase/oxygenase genes as a functional marker for chemolithoautotrophic halophilic sulfur-oxidizing bacteria in hypersaline habitats. Microbiology (UK) 156:2016–2025

    Article  CAS  Google Scholar 

  • Tourova TP, Sorokin DY, Slobodova NV, Bumazhkin BK, Sukhacheva MV (2014) Diversity of diazotrophs in the sediments of saline and soda lakes analyzed with the use of the nifH gene as a molecular marker. Microbiology (Mikrobiologiya) 83:634–647

    Article  CAS  Google Scholar 

  • Tsyrenova DD, Bryanskaya AV, Namsaraev ZB, Akimov VN (2011) Taxonomic and ecological characterization of cyanobacteria from some brackish and saline lakes of Southern Transbaikal Region. Microbiology (Mikrobiologiya) 80:216–227

    Article  CAS  Google Scholar 

  • Vonshak A (1997) Spirulina platensis (Arthrospira) physiology, cell-biology and biotechnology. Taylor & Francis, London. ISBN 0-7484-0674-3

    Google Scholar 

  • Voronikhin NN (1929) Materials for research on the algological vegetation of Kulunda Steppe. Izvestiya Glavnogo Botanicheskogo Sada SSSR 28:12–40 (in Russian)

    Google Scholar 

Download references

Acknowledgements

This work was supported by the Program of fundamental research for state academies (No. 01201350928), Russian Academy of Sciences and Federal Agency of Scientific Organizations (Project Nos. 0104-2018-0033 and 0104-2018-0030). ZN was supported by the NRC “Kurchatov Institute”. DS was supported by the the Gravitation-SIAM program of the Dutch Ministry of Education and Science (24002002).

Author information

Authors and Affiliations

  1. NRC “Kurchatov Institute”, Moscow, 123182, Russia

    Zorigto Namsaraev

  2. Winogradsky Institute of Microbiology, Research Center of Biotechnology RAS, Moscow, 117312, Russia

    Olga Samylina, Dimitry Y. Sorokin & Tatiana Tourova

  3. Institute of Bioengineering, Research Center of Biotechnology RAS, Moscow, 117312, Russia

    Marina Sukhacheva

  4. Soil Science Faculty, Moscow State University, Moscow, 119991, Russia

    Gennadii Borisenko

  5. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands

    Dimitry Y. Sorokin

Authors
  1. Zorigto Namsaraev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Olga Samylina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marina Sukhacheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gennadii Borisenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dimitry Y. Sorokin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tatiana Tourova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zorigto Namsaraev.

Additional information

Communicated by A. Oren.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Namsaraev, Z., Samylina, O., Sukhacheva, M. et al. Effect of salinity on diazotrophic activity and microbial composition of phototrophic communities from Bitter-1 soda lake (Kulunda Steppe, Russia). Extremophiles 22, 651–663 (2018). https://doi.org/10.1007/s00792-018-1026-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-018-1026-7

Keywords

Search

Navigation