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Halophilic Prokaryotes in Urmia Salt Lake, a Hypersaline Environment in Iran

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A Correction to this article was published on 21 July 2021

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Abstract

In this study, fluorescence in situ hybridization (FISH) and PCR-amplified fragments of the 16SrDNA gene were used to determine prokaryotes diversity in Urmia Salt Lake. Prokaryote cell population in Urmia lake range from 3.1 ± 0.3 × 106, 2 ± 0.2 × 108, 4 ± 0.3 × 108, and 1.8 ± 0.2 × 108 cells ml−1 for water, soil, sediment, and salt samples by DAPI (4́, 6-diamidino-2-phenylindole) direct count, respectively. The proportion of bacteria and archaea in the samples determinable by FISH ranged between 36.1 and 55% and 48.5 and 55.5%, respectively. According to the DGGE method, some bands were selected and separated from the gel, then amplified and sequenced. The results of sequences were related to two phyla Proteobacteria (16.6%) and Bacteroidetes (83.3%), which belonged to four genera Salinibacter, Mangroviflexus, Pseudomonas, and Cesiribacter, and the archaeal sequences were related to Euryarchaeota phyla and three genera Halonotius, Haloquadratum, and Halorubrum. According to our results, it seems that prokaryotic populations in this hypersaline environment are more diverse than expected, and bacteria are so abundant and diverse and form the metabolically active part of the microbial population inhabiting this extreme environment. Molecular dependent and independent approaches revealed a different aspect of this environment microbiota.

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References

  1. Boutaiba S, Hacene H, Bidle KA, Maupin-Furlow JA (2011) Microbial diversity of the hypersaline Sidi Ameur and Himalatt Salt Lakes of the Algerian Sahara. J Arid Environ 75(10):909–916

    Article  PubMed  PubMed Central  Google Scholar 

  2. Hedi A, Essghaier B, Cayol JL, Fardeau ML, N, (2014) Prokaryotic biodiversity of halophilic microorganisms isolated from Sehline Sebkha Salt Lake (Tunisia). Afr J Microbiol Res 8(4):355–367

    Article  CAS  Google Scholar 

  3. Oren A, Baxter BK, Weimer BC (2009) Microbial communities in Salt Lakes: Phylogenetic diversity, metabolic diversity, and in situ activities. Nat Resour Environ Issues 15(51):1–8

    Google Scholar 

  4. Ghiasian M, Akhavan Sepahy A, Amoozegar MA, Saadatmand S, Shavandi M (2017) Bacterial diversity determination using culture-dependent and culture-independent methods. Global J Environ Sci Manage 3(2):153–164

    CAS  Google Scholar 

  5. Karło A, Ziembińska A (2013) Modern techniques used for biodiversity analysis in bacterial environmental communities. CHEMIK 67(11):1105–1114

    Google Scholar 

  6. Shipeng Lu, Minjeong P, Hyeon-Su R, Dae Sung L, Woojun P, Jeon CO (2006) Analysis of microbial communities using culture-dependent and culture-independent approaches in an anaerobic/aerobic SBR reactor. J Microbiol 44(2):155–161

    Google Scholar 

  7. Eickhorst T, Tippkotter R (2008) Improved detection of soil microorganisms using fluorescence in situ hybridization (FISH) and catalyzed reporter deposition (CARD-FISH). Soil Biol Biochem 40:1883–1891

    Article  CAS  Google Scholar 

  8. Dastgheib MM, Amoozegar MA, Khajeh K, Shavandi M, Ventosa A (2012) Biodegradation of polycyclic aromatic hydrocarbons by a halophilic microbial consortium. Appl Microbiol Biotechnol 95:789–798

    Article  CAS  PubMed  Google Scholar 

  9. Delgado-García M, Valdivia-Urdiales B, Aguilar-González CN, Contreras-Esquivel JC, Rodríguez-Herrera R (2012) Halophilic hydrolases as a new tool for the biotechnological industries. J Sci Food Agric 92(13):2575–2580

    Article  PubMed  CAS  Google Scholar 

  10. Llamas I, Amjres H, Mata JA, Quesada E, Béjar V (2012) The potential biotechnological applications of the exopolysaccharide produced by the halophilic bacterium Halomonas almeriensis. Molecules 17:7103–7120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Rohban R, Amoozegar MA, Ventosa A (2009) Screening and isolation of halophilic bacteria producing extracellular hydrolyses from Howz Soltan Lake. Iran J Ind Microbiol Biotechnol 36(3):333–340

    Article  CAS  PubMed  Google Scholar 

  12. Tang J, Ai-Ping SP, Bromfield JZ, Shuang-Cheng L, Shi-Quan W, Qi-Ming D, Ping L (2011) 16S rRNA gene sequence analysis of halophilic and halotolerant bacteria isolated from a hypersaline pond in Sichuan, China. Ann Microbiol 61:375–381

    Article  Google Scholar 

  13. Safarpour A, Amoozegar MA, Ventosa, A (2018) Hypersaline environments of Iran: prokaryotic biodiversity and their potentials in microbial biotechnology. Extremophiles in Eurasian Ecosystems. pp 265–298

  14. Jookar Kashi F, Owlia P, Amoozegar MA, Yakhchali B, Kazemi B (2014) Diversity of cultivable microorganisms in the eastern part of Urmia Salt Lake. Iran J Microbiol Biotech Food Sci 4(1):36–43

    Google Scholar 

  15. Jookar Kashi F, Owlia P, Amoozegar MA (2018) Evaluation of prokaryotic diversity in hypersaline environment by culture-independent method. Modares J Biotech 9(1):137–144

    Google Scholar 

  16. Zununi V, Forouhandeh S, Hassanzadeh H, Peter Klenk S, Hejazi H, Hejazi MA (2011) Isolation and characterization of halophilic bacteria from urmia lake in Iran. Microbiology 80(6):834–841

    Article  CAS  Google Scholar 

  17. Mehrshad M, Amoozegar MA, Yakhchali B, Shahzade Fazeli A (2012) Biodiversity of moderately halophilic and halotolerant bacteria in the western coastal line of Urmia lake. Biol J Microorg 2:49–70

    Google Scholar 

  18. Farzin S, Ifaei P, Farzin N, Hassanzadeh Y, Aalami MT (2012) An investigation on changes and prediction of Urmia Lake water surface evaporation by chaos theory. Int J Environ Res 6(3):815–824

    Google Scholar 

  19. Stahl DA, Amann R (1991) Development and application of nucleic acid probes in bacterial systematics. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 205–248

    Google Scholar 

  20. Amann R, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Benlloch S, Acinas SG, Martínez-Mucia AJ, RodríguezValera F (1996) Description of prokaryotic biodiversity along the salinity gradient of a multipond solar saltern by direct PCR amplification of 16S rDNA. Hydrobiologia 329:19–31

    Article  CAS  Google Scholar 

  22. Burns DG, Camakaris HM, Janssen PH, Dyall-Smith ML (2004) Combined use of cultivation-dependent and cultivation independent methods indicates that members of most haloarchaeal groups in an Australian crystallizer pond are cultivable. Appl Environ Microbiol 70:5258–5265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Jookar Kashi F (2016) An improved procedure of the metagenomic DNA extraction from saline soil, sediment and salt. Int Lett Nat Sci 60:38–45

    Google Scholar 

  24. Mutlu MB, Martínez-García M, Santos F, Peña A, Guven K, Antón J (2008) Prokaryotic diversity in Tuz Lake, a hypersaline environment in Inland Turkey. FEMS Microbiol Ecol 65:474–483

    Article  CAS  PubMed  Google Scholar 

  25. Muyzer G, De Waal EC, Uitterrlinden AG (1993) Profiling in complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA, Mcwilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  28. Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor andanalysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:958

    Google Scholar 

  29. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6 (2013) Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–27299.

  30. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791

    Article  PubMed  Google Scholar 

  31. Grant WD (2004) Life at low water activity. Phil Trans R Soc Lond 359:1249–1267

    Article  CAS  Google Scholar 

  32. Jookar Kashi F, Owlia P, Amoozegar MA, Yakhchali B (2014) Culturable prokaryotic diversity of Urmia Salt Lake. Mod Genet 9(38):313–328

    Google Scholar 

  33. Guixa-Boixareu N, Calderón-Paz J, Heldal M, Bratbak G, Pedrós-Alió C (1996) Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat Microbial Ecol 11:215–227

    Article  Google Scholar 

  34. Ochsenreiter T, Pfeifer F, Schleper C (2002) Diversity of Archaea in hypersaline environments characterized by molecular-phylogenetic and cultivation studies. Extremophiles 6:267–274

    Article  CAS  PubMed  Google Scholar 

  35. Antón J, Llobet-Brossa E, Rodriguez-Valera F, Amann R (1999) Fluorescence in situ hybridization analysis of the prokaryotic community inhabiting crystallizer ponds. Environ. Microbiol 5:1517–523

    Google Scholar 

  36. Maturrano L, Santos F, Rossello-Mora R, Anton J (2006) Microbial diversity in Maras salterns, a hypersaline environment in the Peruvian Andes. Appl Environ Microbiol 72:3887–3895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Torsvik V, Lise Daae F, Sandaa RA, Øvreas L (1998) Novel techniques for analysing microbial diversity in natural and perturbed environments. J Biotechnol 664:53–62

    Article  Google Scholar 

  38. Makhdoumi-Kakhki A, Amoozegar MA, Kazemi B, Pašic L, Ventosa A (2012) Prokaryotic diversity in Aran-Bidgol Salt Lake, the largest hypersaline playa in Iran. Microbes Environ 27(1):87–93

    Article  PubMed  Google Scholar 

  39. Didari M, Bagheri M, Amoozegar MA, Bouzari S, Babavalian H, Tebyanian H, Hassanshahian M, Ventosa A (2020) Diversity of halophilic and halotolerant bacteria in the largest seasonal hypersaline lake (Aran-Bidgol-Iran). J Environ Health Sci Eng 87:1–11

    Google Scholar 

  40. Jiaojiao Z, Guannan M, Yuangao D, Jinggang D, Van Gilbert S, Sui L (2016) Bacterial diversity in Bohai Bay Solar Saltworks. China Curr Microbiol 72:55–63

    Article  CAS  Google Scholar 

  41. Nasier A, Sarika S, Farrah GK, Rajinder K, Sarojini J, Malik ZA, Ghulam NQ (2008) Phylogenetic analyses of archaeal ribosomal DNA sequences from Salt Pan Sediment of Mumbai. India Curr Microbiol 57:145–152

    Article  CAS  Google Scholar 

  42. Shuaibing H, Jun T, Wenge H, Chao M (2019) Diversity of archaea and its correlation with environmental factors in the Ebinur Lake Wetland. Curr Microbiol 76:1417–1424

    Article  CAS  Google Scholar 

  43. Swapnil K, Neelima D, Yogesh S, Avinash S (2020) Cultivation of diverse microorganisms from hypersaline lake and impact of delay in sample processing on cell viability. Curr Microbiol 77:716–721

    Article  CAS  Google Scholar 

  44. Cycil LM, DasSarma S, Pecher W, McDonald R, AbdulSalam M, Hasan F (2020) Metagenomic insights into the diversity of halophilic microorganisms indigenous to the Karak Salt Mine. Pakistan Front Microbiol 11:1567

    Article  PubMed  Google Scholar 

  45. Derui Z, Rui H, Qifu L, Xiang G, Jiangwa X, Guoping S, Yongzhen L, Rong W (2020) An evaluation of the core bacterial communities associated with hypersaline environments in the Qaidam Basin. China Arch Microbiol 202(8):2093–2103

    Article  CAS  Google Scholar 

  46. Shaoxing C, Yao X, Libby H (2020) Geographical isolation, buried depth, and physicochemical traits drive the variation of species diversity and prokaryotic community in three typical hypersaline environments. Microorganisms 8(120):1–14

    Google Scholar 

  47. Zhang L, CAI Y, Jiang M, Dai J, Guo X, LI W, LI Y. (2020) The levels of microbial diversity in different water layers of saline Chagan Lake. China J Oceanol Limnol 38:395–407

    Article  CAS  Google Scholar 

  48. De Mandal S, Panda AK, Bisht SS, Kumar NS (2015) Microbial ecology in the era of next generation sequencing. Next Generat Seq Appl 21:1–6

    Google Scholar 

  49. Raquel AC, Victor HS, Gretty KV (2018) Microbial diversity assessment by PCR-DGGE analysis in national sanctuary of ampay in Perú. Adv Appl Microbiol 11(3):1–6

    Google Scholar 

  50. Samarajeewa AD, Hammad A, Masson L, Khan IUH, Scroggins R, Beaudette LA (2015) Comparative assessment of next-generation sequencing, denaturing gradient gel electrophoresis, clonal restriction fragment length polymorphism and cloning-sequencing as methods for characterizing commercial microbial consortia. J Microbiol Methods 108:103–111

    Article  CAS  PubMed  Google Scholar 

  51. Matthias S, Robert G, Sebastian T (2020) Environmental degradation at Lake Urmia (Iran): exploring the causes and their impacts on rural livelihoods. GeoJournal 8:1–15

    Google Scholar 

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The authors are grateful to Shahed University for supporting this work.

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Correspondence to Fereshteh Jookar Kashi.

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Jookar Kashi, F., Owlia, P., Amoozegar, M.A. et al. Halophilic Prokaryotes in Urmia Salt Lake, a Hypersaline Environment in Iran. Curr Microbiol 78, 3230–3238 (2021). https://doi.org/10.1007/s00284-021-02583-w

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