Skip to main content
SpringerLink
Log in

Soda pans of the Pannonian steppe harbor unique bacterial communities adapted to multiple extreme conditions

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

Abstract

Soda pans of the Pannonian steppe are unique environments regarding their physical and chemical characteristics: shallowness, high turbidity, intermittent character, alkaline pH, polyhumic organic carbon concentration, hypertrophic condition, moderately high salinity, sodium and carbonate ion dominance. The pans are highly productive environments with picophytoplankton predominance. Little is known about the planktonic bacterial communities inhabiting these aquatic habitats; therefore, amplicon sequencing and shotgun metagenomics were applied to reveal their composition and functional properties. Results showed a taxonomically complex bacterial community which was distinct from other soda lakes regarding its composition, e.g. the dominance of class Alphaproteobacteria was observed within phylum Proteobacteria. The shotgun metagenomic analysis revealed several functional gene components related to the harsh and at the same time hypertrophic environmental conditions, e.g. proteins involved in stress response, transport and hydrolase systems targeting phytoplankton-derived organic matter. This is the first detailed report on the indigenous planktonic bacterial communities coping with the multiple extreme conditions present in the unique soda pans of the Pannonian steppe.

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

Similar content being viewed by others

References

  • Anil Kumar P, Srinivas TN, Madhu S et al (2010) Indibacter alkaliphilus gen. nov., sp. nov., an alkaliphilic bacterium isolated from a haloalkaline lake. Int J Syst Evol Microbiol 60:721–726

    Article  CAS  PubMed  Google Scholar 

  • Antony CP, Kumaresan D, Hunger S, Drake HL et al (2013) Microbiology of Lonar Lake and other soda lakes. ISME J 7:468–476

    Article  PubMed  Google Scholar 

  • Atanasova NS, Oksanen HM, Bamford DH (2015) Haloviruses of archaea, bacteria, and eukaryotes. Curr Opin Microbiol 25:40–48

    Article  PubMed  Google Scholar 

  • Banciu HL, Muntyan MS (2015) Adaptive strategies in the double-extremophilic prokaryotes inhabiting soda lakes. Curr Opin Microbiol 25:73–79

    Article  CAS  PubMed  Google Scholar 

  • Blankenberg D, Kuster GV, Coraor N et al. (2010) Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol. doi:10.1002/0471142727.mb1910s89

    PubMed  PubMed Central  Google Scholar 

  • Boros E, Nagy T, Pigniczki Cs et al (2008) The effect of aquatic birds on the nutrient load and water quality of soda pans in Hungary. Acta Zool Hung 54:207–224

    Google Scholar 

  • Boros E, Horváth Zs, Wolfram G et al (2014) Salinity and ionic composition of the shallow soda pans in the Carpathian Basin. Ann Limnol Int J Lim 50:59–69

    Article  Google Scholar 

  • Boros E, Pigniczki Cs, Sápi T et al (2016) Waterbird-mediated productivity of two soda pans in the Carpathian Basin in Central Europe. Waterbirds 39:388–401

    Article  Google Scholar 

  • Boros E, Balogh KV, Vörös L et al (2017) Multiple extreme environmental conditions of intermittent soda pans in the Carpathian Basin (Central Europe). Limnologica 62:38–46

    Article  CAS  Google Scholar 

  • Borsodi AK, Knáb M, Czeibert K et al (2013) Planktonic bacterial community composition of an extremely shallow soda pond during a phytoplankton bloom revealed by cultivation and molecular cloning. Extremophiles 17:575–584

    Article  PubMed  Google Scholar 

  • Brenner DJ, Krieg NR, Staley JT (2005) Bergey’s manual of systematic bacteriology, the Proteobacteria, 2nd edn. Springer, New York

    Book  Google Scholar 

  • Buchan A, LeCleir GR, Gulvik CA et al (2014) Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12:686–698

    Article  CAS  PubMed  Google Scholar 

  • Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60

    Article  CAS  PubMed  Google Scholar 

  • Cai M, Wang L, Cai H et al (2011) Salinarimonas ramus sp. nov. and Tessaracoccus oleiagri sp. nov., isolated from a crude oil-contaminated saline soil. Int J Syst Evol Microbiol 61:1767–1775

    Article  CAS  PubMed  Google Scholar 

  • Chiu HH, Rogozin DY, Huang SP et al (2014) Aliidiomarina shirensis sp. nov., a halophilic bacterium isolated from Shira Lake in Khakasia, southern Siberia, and a proposal to transfer Idiomarina maris to the genus Aliidiomarina. Int J Syst Evol Microbiol 64:1334–1339

    Article  CAS  PubMed  Google Scholar 

  • Dimitriu PA, Pinkart HC, Peyton BM et al (2008) Spatial and temporal patterns in the microbial diversity of a meromictic soda lake in Washington State. Appl Environ Microbiol 74:4877–4888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doronina N, Kaparullina E, Trotsenko Y (2014) The Family Methylophilaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson T (eds) The Prokaryotes: Alphaproteobacteria and Betaproteobacteria, 4th edn. Springer, Berlin, pp 869–880

    Chapter  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eiler A, Zaremba-Niedzwiedzka K, Martínez-García M et al (2014) Productivity and salinity structuring of the microplankton revealed by comparative freshwater metagenomics. Environ Microbiol 16:2682–2698

    Article  CAS  PubMed  Google Scholar 

  • Felföldi T, Somogyi B, Márialigeti K et al (2009) Characterization of photoautotrophic picoplankton assemblages in turbid, alkaline lakes of the Carpathian Basin (Central Europe). J Limnol 68:385–395

    Article  Google Scholar 

  • Felföldi T, Somogyi B, Márialigeti K et al (2011) Notes on the biogeography of non-marine planktonic picocyanobacteria: re-evaluating novelty. J Plankton Res 33:1622–1626

    Article  Google Scholar 

  • Foti M, Sorokin DY, Lomans B et al (2007) Diversity, activity, and abundance of sulfate-reducing bacteria in saline and hypersaline soda lakes. Appl Environ Microbiol 73:2093–2100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giardine B, Riemer C, Hardison RC et al (2005) Galaxy: a platform for interactive large-scale genome analysis. Genome Res 15:1451–1455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goecks J, Nekrutenko A, Taylor J (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11:R86

    Article  PubMed  PubMed Central  Google Scholar 

  • Goodfellow M, Kämpfer P, Busse HJ et al (2012) Bergey’s manual of systematic bacteriology, the Actinobacteria, 2nd edn. Springer, New York

    Book  Google Scholar 

  • Grant WD (2004) Half a lifetime in Soda lakes. In: Vantosa A (ed) Halophilic microorganisms. Springer, Berlin, pp 17–31

    Chapter  Google Scholar 

  • Hammer UT (1986) Saline lake ecosystems of the world, vol 59. Springer, New York, p 15

    Google Scholar 

  • Huson DH, Auch AF, Qi J et al (2007) MEGAN analysis of metagenomic data. Genome Res 17:377–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung YT, Park S, Lee JS et al (2006) Altererythrobacter aestiaquae sp. nov., isolated from seawater. Int J Syst Evol Microbiol 64:3943–3949

    Article  Google Scholar 

  • Kalyuzhnaya MG, Bowerman S, Lara JC et al (2006) Methylotenera mobilis gen. nov., sp. nov., an obligately methylamine-utilizing bacterium within the family Methylophilaceae. Int J Syst Evol Microbiol 56:2819–2823

    Article  CAS  PubMed  Google Scholar 

  • Kirchman DL (2002) The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39:91–100

    CAS  PubMed  Google Scholar 

  • Klindworth A, Pruesse E, Schweer T et al (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1

    Article  CAS  PubMed  Google Scholar 

  • Krieg NR, Staley JT, Brown DR et al (2010) Bergey’s manual of systematic bacteriology, the Bacteroidetes, Spirochaetes, Tenericutes, (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes, 2nd edn. Springer, New York

    Google Scholar 

  • Krienitz L, Kotut K (2010) Fluctuating algal food populations and the occurrence of Lesser Flamingos (Phoeniconaias minor) in three Kenyan Rift Valley lakes. J Phycol 46:1088–1096

    Article  Google Scholar 

  • Krulwich TA, Sachs G, Padan E (2011) Molecular aspects of bacterial pH sensing and homeostasis. Nat Rev Microbiol 9:330–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kunin V, Engelbrektson A, Ochman H et al (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12:118–123

    Article  CAS  PubMed  Google Scholar 

  • Lanzén A, Simachew A, Gessesse A et al (2013) Surprising prokaryotic and eukaryotic diversity, community structure and biogeography of Ethiopian soda lakes. PLoS One 8:e72577

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu YP, Wang YX, Li YX et al (2005) Mongoliicoccus roseus gen. nov., sp. nov., an alkaliphilic bacterium isolated from a haloalkaline lake. Int J Syst Evol Microbiol 62:2206–2212

    Article  Google Scholar 

  • Lott SC, Voß B, Hess WR et al (2015) CoVennTree: a new method for the comparative analysis of large datasets. Front Genet 6:43

    Article  PubMed  PubMed Central  Google Scholar 

  • Meyer F, Paarmann D, D’Souza M et al (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform 9:386

    Article  CAS  Google Scholar 

  • Mühling M, Fuller NJ, Millard A et al (2005) Genetic diversity of marine Synechococcus and co-occurring cyanophage communities: evidence for viral control of phytoplankton. Environ Microbiol 7:499–508

    Article  PubMed  Google Scholar 

  • Mulkidjanian AY, Dibrov P, Galperin MY (2008) The past and present of sodium energetics: may the sodium-motive force be with you. BBA-Bioenerg 1777:985–992

    Article  CAS  Google Scholar 

  • Muntyan MS, Cherepanov DA, Malinen AM et al (2015) Cytochrome cbb3 of Thioalkalivibrio is a Na+-pumping cytochrome oxidase. Proc Natl Acad Sci 112:7695–7700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oh S, Caro-Quintero A, Tsementzi D et al (2011) Metagenomic insights into the evolution, function, and complexity of the planktonic microbial community of Lake Lanier, a temperate freshwater ecosystem. Appl Environ Microbiol 77:6000–6011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pálffy K, Felföldi T, Mentes A et al (2014) Unique picoeukaryotic algal community under multiple environmental stress conditions in a shallow, alkaline pan. Extremophiles 18:111–119

    Article  PubMed  Google Scholar 

  • Paul D, Kumbhare SV, Mhatre SS et al (2016) Exploration of microbial diversity and community structure of Lonar Lake: the only hypersaline meteorite crater lake within basalt rock. Front Microbiol 6:1553

    Article  PubMed  PubMed Central  Google Scholar 

  • Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl Acids Res 41:D590–D596

    Article  CAS  PubMed  Google Scholar 

  • Raven JA (1998) The twelfth Tansley lecture. Small is beautiful: the picophytoplankton. Funct Ecol 12:503–513

    Article  Google Scholar 

  • Reyes-Prieto A, Barquera B, Juarez O (2014) Origin and evolution of the sodium-pumping NADH: ubiquinone oxidoreductase. PLoS One 9:e96696

    Article  PubMed  PubMed Central  Google Scholar 

  • Satomi M, Kimura B, Hamada T et al (2002) Phylogenetic study of the genus Oceanospirillum based on 16S rRNA and gyrB genes: emended description of the genus Oceanospirillum, description of Pseudospirillum gen. nov., Oceanobacter gen. nov. and Terasakiella gen. nov. and transfer of Oceanospirillum jannaschii and Pseudomonas stanieri to Marinobacterium as Marinobacterium jannaschii comb. nov. and Marinobacterium stanieri comb. nov. Int J Syst Evol Microbiol 52:739–747

    CAS  PubMed  Google Scholar 

  • Schagerl M, Burian A, Gruber-Dorninger M et al (2015) Algal communities of Kenyan soda lakes with a special focus on Arthrospira fusiformis. Fottea 15:245–257

    Article  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shannon P, Markiel A, Ozier O et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Somogyi B, Felföldi T, Vanyovszki J et al (2009) Winter bloom of picoeukaryotes in Hungarian shallow turbid soda pans and the role of light and temperature. Aquat Ecol 43:735–744

    Article  CAS  Google Scholar 

  • Somogyi B, Felföldi T, Dinka M et al (2010) Periodic picophytoplankton predominance in a large, shallow alkaline lake (Lake Fertő/Neusiedlersee). Ann Limnol Int J Lim 46:9–19

    Article  Google Scholar 

  • Somogyi B, Felföldi T, Solymosi K et al (2011) Chloroparva pannonica gen. et sp. nov. (Trebouxiophyceae, Chlorophyta)—a new picoplanktonic green alga from a turbid, shallow soda pan. Phycologia 50:1–10

    Article  CAS  Google Scholar 

  • Somogyi B, Felföldi T, V.-Balogh K et al (2016) The role and composition of winter picoeukaryotic assemblages in shallow lakes. J Great Lakes Res 42:1420–1431

    Article  Google Scholar 

  • Sorokin DY, Berben T, Melton ED et al (2014) Microbial diversity and biogeochemical cycling in soda lakes. Extremophiles 18:791–809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Teeling H, Fuchs BM, Becher D et al (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336:608–611

    Article  CAS  PubMed  Google Scholar 

  • Tindall BJ, Rossello-Mora R, Busse H-J et al (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266

    Article  CAS  PubMed  Google Scholar 

  • Van Trappen S, Mergaert J, Swings J (2004) Loktanella salsilacus gen. nov., sp. nov., Loktanella fryxellensis sp. nov. and Loktanella vestfoldensis sp. nov., new members of the Rhodobacter group, isolated from microbial mats in Antarctic lakes. Int J Syst Evol Microbiol 54:1263–1269

    Article  PubMed  Google Scholar 

  • Vavourakis CD, Ghai R, Rodriguez-Valera F et al (2016) Metagenomic insights into the uncultured diversity and physiology of microbes in four hypersaline soda lake brines. Front Microbiol 7:211

    Article  PubMed  PubMed Central  Google Scholar 

  • V.-Balogh K, Németh B, Vörös L (2009) Specific attenuation coefficients of optically active substances and their contribution to the underwater ultraviolet and visible light climate in shallow lakes and ponds. Hydrobiologia 632:91–105

    Article  CAS  Google Scholar 

  • Vörös L, Somogyi B, Boros E (2008) Birds cause net heterotrophy in shallow lakes. Acta Zool Acad Sci Hung 54:23–34

    Google Scholar 

  • Vörös L, Mózes A, Somogyi B (2009) A five-year study of autotrophic winter picoplankton in Lake Balaton, Hungary. Aquat Ecol 43:727–734

    Article  Google Scholar 

  • Weisse T (1993) Dynamics of autotrophic picoplankton in marine and freshwater ecosystems. Adv Microb Ecol 13:327–370

    Article  Google Scholar 

  • Wilhelm SW, Suttle CA (1999) Viruses and nutrient cycles in the sea. Bioscience 49:781–788

    Article  Google Scholar 

  • Williams TJ, Wilkins D, Long E et al (2013) The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. Environ Microbiol 15:1302–1317

    Article  CAS  PubMed  Google Scholar 

  • Xing P, Hahnke RL, Unfried F et al (2015) Niches of two polysaccharide-degrading Polaribacter isolates from the North Sea during a spring diatom bloom. ISME J 9:1410–1422

    Article  CAS  PubMed  Google Scholar 

  • Yoon JH, Kang SJ, Lee SY et al (2009) Seohaeicola saemankumensis gen. nov., sp. nov., isolated from a tidal flat. Int J Syst Evol Microbiol 59:2675–2679

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are thankful to Emil Boros, Balázs Németh and Tamás Sápi for their assistance during sampling. We are thankful to Annamária Kéri and János Kubisch for their help in establishing the computational environment for the CoVennTree program.

Author information

Authors and Affiliations

  1. Department of Microbiology, Eötvös Loránd University, Pázmány Péter stny. 1/C, 1117, Budapest, Hungary

    Attila Szabó, Kristóf Korponai, Károly Márialigeti & Tamás Felföldi

  2. Institute for Computer Science and Control, Hungarian Academy of Sciences (MTA SZTAKI), Kende u. 13-17, 1111, Budapest, Hungary

    Csaba Kerepesi

  3. MTA Centre for Ecological Research, Balaton Limnological Institute, Klebelsberg Kunó u. 3, 8237, Tihany, Hungary

    Boglárka Somogyi & Lajos Vörös

  4. Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungarian Academy of Sciences, Hungária krt. 21, 1143, Budapest, Hungary

    Dániel Bartha

Authors
  1. Attila Szabó
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kristóf Korponai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Csaba Kerepesi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Boglárka Somogyi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lajos Vörös
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dániel Bartha
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Károly Márialigeti
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tamás Felföldi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tamás Felföldi.

Ethics declarations

Funding

This work was financially supported by the Hungarian Scientific Research Fund (Grants OTKA PD105407, PD112449); the Momentum Grant of the Hungarian Academy of Sciences (LP2012-19/2012) to CS.K, and the Bolyai János Research Grant (Hungarian Academy of Sciences) to B.S and T.F. Purchase of equipment was financed by the National Development Agency (Grants KMOP-4.2.1/B-10-2011-0002, TÁMOP-4.2.2/B-10/1-2010-0030).

Additional information

Communicated by A. Oren.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Szabó, A., Korponai, K., Kerepesi, C. et al. Soda pans of the Pannonian steppe harbor unique bacterial communities adapted to multiple extreme conditions. Extremophiles 21, 639–649 (2017). https://doi.org/10.1007/s00792-017-0932-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-017-0932-4

Keywords

Search

Navigation