Advertisement

Microbiology

, Volume 87, Issue 4, pp 569–582 | Cite as

Diversity of Prokaryotes in Planktonic Communities of Saline Sol-Iletsk lakes (Orenburg Oblast, Russia)

  • E. A. SelivanovaEmail author
  • D. V. Poshvina
  • Yu. A. Khlopko
  • N. E. Gogoleva
  • A. O. Plotnikov
Experimental Articles

Abstract

Prokaryotic diversity was studied in the planktonic communities of six Sol-Iletsk lakes (Orenburg oblast, Russia) varying in salinity level using the Illumina technology of high-throughput sequencing. The extremely halophilic archaea of the phyla Euryarchaeota and Nanohaloarchaeota, as well as the bacterial phylum Bacteroidetes predominated in the communities of lakes with salinity of 285–300‰. Representatives of the phyla Bacteroidetes and Actinobacteria, as well as of the class Gammaproteobacteria were predominant in the lakes with salinity 110−180‰. A bloom of Cyanobacteria was observed in Bol’shoe Gorodskoe Lake (10‰ salinity). The dominant OTUs in the lakes with high salinity were represented by archaea Halonotius sp., uncultured Nanohaloarchaea, and bacteria Salinibacter sp. In the lakes with medium salinity level the dominants included gammaproteobacteria Spiribacter sp., alphaproteobacteria Roseovarius sp., flavobacteria Psychroflexus sp., unidentified archaea of the family Haloferacaceae, actinobacteria Pontimonas sp. and Rhodoluna sp. In the lake with low salinity level cyanobacteria of the genus Planktothrix were predominant. Effect of salinity on prokaryotic taxonomic richness, composition, and diversity in planktonic communities of the studied lakes was demonstrated.

Keywords

saline lakes biodiversity prokaryotes halophilic bacteria archaea planktonic communities high-throughput sequencing Illumina 16S rRNA gene 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abdrakhmanov, A.R., Abdrakhmanov, A.R., and Butkova, G.A., Mineral’nye i gryazevye ozera Sol’-Iletska (Sol-Iletsk Mineral and Mud Lakes), Sol-Iletsk, 2005.Google Scholar
  2. Abdrakhmanov, A.R., Microflora of a saline Lake (Lake Razval, Orenburg oblast), Extended Abstract Cand. Sci. (Med.) Dissertation, Orenburg: Orenburg State Med. Acad., 2001.Google Scholar
  3. Anton, J., Oren, A., Benlloch, S., Rodriguez-Valera, F., Amann, R., and Rossello-Mora, R., Salinibacter ruber gen. nov., sp. nov., a novel, extremely halophilic member of the Bacteria from saltern crystallizer ponds, Int. J. Syst. Evol. Microbiol., 2002, vol. 52, pp. 485–491.CrossRefPubMedGoogle Scholar
  4. Baati, H., Guermazi, S., Gharsallah, N., Sghir, A., and Ammar, E., Novel prokaryotic diversity in sediments of Tunisian multipond solar saltern, Res. Microbiol., 2010, vol. 161, pp. 573–582.CrossRefPubMedGoogle Scholar
  5. Bel’kova, N.L., A modified method for total DNA isolation from water samples and soil extracts by enzymatic lysis, in Molekulyarno-geneticheskie metody analiza mikrobnykh soobshchestv. Raznoobrazie mikrobnykh soobshchestv vnutrennikh vodoemov Rossii (Molecular Genetic Methods for Analysis of Microbial Communities. Diversity of Microbial Communities of Russian Inland Waters), Yaroslavl: Printhaus, 2009, pp. 53–63.Google Scholar
  6. Blyumina, L.S., Biology of Sol-Iletsk saline Lakes, Extended Abstract Cand. Sci. (Biol.) Dissertation, Orenburg: Orenburg Med. Inst., 1958.Google Scholar
  7. DeMaere, M.Z., Williams, T.J., Allen, M.A., Brown, M.V., Gibson, J.A., Rich, J., Lauro, F.M., Dyall-Smith, M., Davenport, K.W., Woyke, T., Kyrpides, N.C., Tringe, S.G., and Cavicchioli, R., High level of intergenera gene exchange shapes the evolution of haloarchaea in an isolated Antarctic Lake, Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, pp. 16939–16944.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Dillon, J.G., Carlin, M., Gutierrez, A., Nguyen, V. and McLain, N., Patterns of microbial diversity along a salinity gradient in the Guerrero Negro solar saltern, Baja CA Sur, Mexico, Front. Microbiol., 2013, vol. 4. 399. eCollection 2013. doi 10.3389/fmicb.2013.00399Google Scholar
  9. Edgar, R.C., Search and clustering orders of magnitude faster than BLAST, Bioinformatics, 2010, vol. 26, pp. 2460–2461.CrossRefPubMedGoogle Scholar
  10. Edgar, R.C., UPARSE: highly accurate OTU sequences from microbial amplicon reads, Nature Methods, 2013, vol. 10, pp. 996–998.CrossRefPubMedGoogle Scholar
  11. Fernández, A.B., León, M.J., Vera, B., Sánchez-Porro, C., and Ventosa, A., Metagenomic sequence of prokaryotic microbiota from an intermediate-salinity pond of a saltern in Isla Cristina, Spain, Genome Announc., 2014, vol. 2, no. 1. pii: e00045-14. doi 10.1128/genomeA.00045-14Google Scholar
  12. Ghai, R., Pasic, L., Fernandez, A.B., Martin-Cuadrado, A.B., Mizuno, C.M., McMahon, K.D., Papke, R.T., Stepanauskas, R., Rodriguez-Brito, B., Rohwer, F., Sanchez-Porro, C., Ventosa, A., and Rodriguez-Valera, F., New abundant microbial groups in aquatic hypersaline environments, Sci. Rep., 2011. 1:135. doi 10.1038/srep00135Google Scholar
  13. Hammer, O., Harper, D.A.T., and Ryan, P.D., PAST: Paleontological Statistic software package for education and data analysis, Paleontologia Electronica 2001, vol. 4, no. 1, pp. 1–9. http://palaeoelectronica.org/2001_1/past/issue1_01.htm. Accessed: 04/X/2011.Google Scholar
  14. Harding, T., Brown, M.W., Plotnikov, A., Selivanova, E., Park, J.S., Gunderson, J.H., Baumgartner, M., Silberman, J.D., Roger, A.J., and Simpson, A.G., Amoeba stages in the deepest branching heteroloboseans, including Pharyngomonas: evolutionary and systematic implications, Protist, 2013, vol. 164, pp. 272–286.CrossRefPubMedGoogle Scholar
  15. Humayoun, S.B., Bano, N., and Hollibaugh, J.T., Depth distribution of microbial diversity in Mono Lake, a meromictic soda Lake in California, Appl. Environ. Microbiol., 2003, vol. 69, pp. 1030–1042.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Huse, S.M., Mark, Welch, D.B., Voorhis, A., Shipunova, A., Morrison, H.G., Eren, A.M., and Sogin, M.L., VAMPS: a website for visualization and analysis of microbial population structures, BMC Bioinform., 2014, vol. 41. doi 10.1186/1471-2105-15-41Google Scholar
  17. Jang, G.I., Cho, Y., and Cho, B.C., Pontimonas salivibrio gen. nov., sp. nov., a new member of the family Microbacteriaceae isolated from a seawater reservoir of a solar saltern, Int. J. Syst. Evol. Microbiol., 2013, vol. 63, pp. 2124–2131.CrossRefPubMedGoogle Scholar
  18. Jookar, Kashi, F., Owlia, P., Amoozegar, M.A., and Yakhchali, B., Culturable prokaryotic diversity of Urmia salt Lake, Modern Genetics J., 2014, vol. 9, no. 3 (38), pp. 313–328.Google Scholar
  19. Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., and Glöckner, F.O., Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies, Nucleic Acids Res., 2013, vol. 41, no. 1. e1. doi 10.1093/nar/gks808Google Scholar
  20. Legault, B.A., Lopez-Lopez, A., Alba-Casado, J.C., Doolittle, W.F., Bolhuis, H., Rodriguez-Valera, F., and Papke, R.T., Environmental genomics of “Haloquadratum walsbyi” in a saltern crystallizer indicates a large pool of accessory genes in an otherwise coherent species, BMC Genomics, 2006, vol. 7, no. 171. doi 10.1186/1471-2164-7-171Google Scholar
  21. Leon, M.J., Fernandez, A.B., Ghai, R., Sanchez-Porro, C., Rodriguez-Valera, F., and Ventosa, A., From metagenomics to pure culture: isolation and characterization of the moderately halophilic bacterium Spiribacter salinus gen. nov., sp. nov., Appl. Environ. Microbiol., 2014, vol. 80, pp. 3850–3857.CrossRefPubMedPubMedCentralGoogle Scholar
  22. León, M.J., Vera-Gargallo, B., Sanchez-Porro, C., and Ventosa, A., Spiribacter roseus sp. nov., a moderately halophilic species of the genus Spiribacter from salterns, Int. J. Syst. Evol. Microbiol., 2016, vol. 66, pp. 4218–4224.CrossRefPubMedGoogle Scholar
  23. Llirós, M., Trias, R., Borrego, C., and Bañeras, L., Specific archaeal communities are selected on the root surfaces of Ruppia spp. and Phragmites australis, Soc. Wetland Sci., 2013. doi 10.1007/s13157-013-0507-9Google Scholar
  24. Myl’nikov, A.P., Percolomonas lacustris sp. nov. (Excavata, Percolozoa), a new flagellate from a continental saline Lake (southeastern European Russia), Zool. Zh., 2015, vol. 94, no. 4, pp. 375–382.Google Scholar
  25. Naghoni, A., Emtiazi, G., Amoozegar, M.A., Cretoiu, M.S., Sta, L.J., Etemadifar, Z., Fazeli, S.A.S., and Bolhuis, H., Microbial diversity in the hypersaline Lake Meyghan, Iran, Sci. Rep., 2017, vol. 7. 11522. doi 10.1038/s41598-017-11585-3Google Scholar
  26. Nelson, W.C. and Stegen, J.C., The reduced genomes of Parcubacteria (OD1) contain signatures of a symbiotic lifestyle, Front. Microbiol., 2015, vol. 6. 713. eCollection 2015. doi 10.3389/fmicb.2015.00713Google Scholar
  27. Nemtseva, N.V., Selivanova, E.A., Ignatenko, M.E., and Sharapova, N.V., Characterization of a novel Dunaliella salina (Chlorophyta) strain and the assessment of its cultivation parameters, Russ. J. Plant Physiol., vol. 60, pp. 529–535. doi 10.3389/fmicb.2015.00713Google Scholar
  28. Oliveros, J.C., Venny. An interactive tool for comparing lists with Venn’s diagrams, 2015. http://bioinfogp.cnb. csic.es/tools/venny/index.html.Google Scholar
  29. Oren A. Taxonomy of halophilic Archaea: current status and future challenges, Extremophiles, 2014, vol. 18, pp. 825–834.CrossRefPubMedGoogle Scholar
  30. Pagaling, E., Wang, H., Venables, M., Wallace, A., Grant, W.D., Cowan, D.A., Jones, B.E., Ma, Y., Ventosa, A., and Heaphy, S., Microbial biogeography of six salt Lakes in Inner Mongolia, China, and a salt Lake in Argentina, Appl. Environ. Microbiol., 2009, vol. 75, pp. 5750–5760.Google Scholar
  31. Pavlov, A.O., Otchet of detal’noi razvedke lechebnykh gryazei ozer Tuzluchnoe i Dunino, a takzhe po izucheniyu rapy ozera Razval dlyz obespecheniya gryazevymi i rapnymi resursami Sol’-Iletskoi kurortnoi zony Orenburgskoi oblasti (Report on Detailed Prospecting of Medicinal Muds of Lakes Tuzluchnoe and Dunino, and on Investigation of Lake Razval Brine for Provision of Mud and Brine Resources for the Sol-Iletsk Resort Zone, Orenburg Oblast), Moscow, 1993.Google Scholar
  32. Petrishchev, V.P., Salt dome landscapes: problems of rational utilization of natural resources of nuclear geosystems, Almanakh Molodoi Nauki, 2015, no. 4, pp. 14–2.Google Scholar
  33. Petrishchev, V.P., Salt dome morphostructures of Southern Ural area, Geomorphologiya, 2010, no. 1, pp. 86–94.Google Scholar
  34. Plotnikov, A.O., Mechanisms of formation of protozoanbacterial associations in aquatic ecosystems (experimental study), Extended Abstract Cand. Sci. (Med.) Dissertation, Orenburg: Orenburg State Med. Acad., 2002.Google Scholar
  35. Plotnikov, A.O., Myl’nikov, A.P., and Selivanova, E.A., Morphology and life cycle of the amoebaflagellate Pharyngomonas sp. (Heterolobosea, Excavata) from a hyperhaline continental Lake Razval, Zool. Zh., 2015, vol. 94, no. 3, pp. 275–286.Google Scholar
  36. Plotnikov, A.O., Selivanova, E.A., and Nemtseva, N.B., Species composition of heterotrophic flagellates from Sol-Iletsk saline Lakes, Izv. Penz. Gos. Ped. Univ., 2011, no. 25, pp. 577–586.Google Scholar
  37. Selivanova, E.A. and Nemtseva, N.V., Experimental interaction of halophilic prokaryotes and opportunistic pathogenic bacteria in brine, Zh. Mikrobiol. Epidemiol. Immunobiol., 2013, no. 5, pp. 86–91.Google Scholar
  38. Selivanova, E.A., Symbiotic associations of microorganisms in planktonic communities of saline Lakes, Extended Abstract Cand. Sci. (Med.) Dissertation, Orenburg: Orenburg State Med. Acad., 2007.Google Scholar
  39. Shabanov, S.V., Biological role of antilysozyme activity in algae, Extended Abstract Cand. Sci. (Med.) Dissertation, Orenburg: Orenburg State Med. Acad., 2001.Google Scholar
  40. Solovchenko, A.E., Chekanov, K.A., Lobakova, E.S., Sidorov, R.A., Selivanova, E.A., and Nemtseva, N.V., Induction of secondary carotenogenesis in new halophile microalgae from the genus Dunaliella (Chlorophyceae), Biochemistry (Moscow), 2015, vol. 80, pp. 1508–1513.CrossRefGoogle Scholar
  41. Sorensen, K.B. and Teske, A., Stratified communities of active Archaea in deep marine subsurface sediments, Appl. Environ. Microbiol., 2006, vol. 72, pp. 4596–4603.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Suda, S., Watanabe, M.M., Otsuka, S., Mahakahant, A., Yongmanitchai, W., Nopartnaraporn, N., Liu, Y., and Day, J.G., Taxonomic revision of water-bloom-forming species of oscillatorioid cyanobacteria, Int. J. Syst. Evol. Microbiol., 2002, vol. 52, pp. 1577–1595.PubMedGoogle Scholar
  43. Tazi, L., Breakwell, D.P., Harker, A.R., and Crandall, K.A., Life in extreme environments: microbial diversity in Great Salt Lake, Utah, Extremophiles, 2014, vol. 18, pp. 525–535.CrossRefPubMedGoogle Scholar
  44. Teske, A. and Sorensen, K.B., Uncultured archaea in deep marine subsurface sediments: have we caught them all?, ISME J., 2008, vol. 2, pp. 3–18.CrossRefPubMedGoogle Scholar
  45. Trigui, H., Masmoudi, S., Brochier-Armanet, C., Barani, A., Gregori, G., Denis, M., Dukan, S., and Maalej, S., Characterization of heterotrophic prokaryote subgroups in the Sfax coastal solar salterns by combining flow cytometry cell sorting and phylogenetic analysis, Extremophiles, 2011, vol. 15, pp. 347–358.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Zhang, J., Kobert, K., Flouri, T., and Stamatakis, A., PEAR: a fast and accurate Illumina Paired-End reAd merger, Bioinformatics, 2014, vol. 30, pp. 614–620.CrossRefPubMedGoogle Scholar
  47. Zhang, R., Wu, Q., Piceno, Y.M., Desantis, T.Z., Saunders, F.M., Andersen, G.L., and Liu, W.T., Diversity of bacterioplankton in contrasting Tibetan Lakes revealed by high-density microarray and clone library analysis, FEMS Microbiol. Ecol., 2013, vol. 86, pp. 277–287.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • E. A. Selivanova
    • 1
    Email author
  • D. V. Poshvina
    • 1
  • Yu. A. Khlopko
    • 1
  • N. E. Gogoleva
    • 2
    • 3
  • A. O. Plotnikov
    • 1
  1. 1.Institute for Cellular and Intracellular Symbiosis, Ural BranchRussian Academy of SciencesOrenburgRussia
  2. 2.Kazan Institute of Biochemistry and BiophysicsRussian Academy of SciencesKazanRussia
  3. 3.Kazan Federal UniversityKazanRussia

Personalised recommendations