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Spatial and temporal distribution of archaeal diversity in meromictic, hypersaline Ocnei Lake (Transylvanian Basin, Romania)

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Abstract

Saline, meromictic lakes with significant depth are usually formed as a result of salt mining activity. Ocnei Lake is one of the largest Transylvanian (Central Romania) neutral, hypersaline lake of man-made origin. We aimed to survey the seasonal dynamics of archaeal diversity in the water column of Ocnei Lake by employing microbiological methods as well as molecular techniques based on the sequence analysis of the 16S rRNA gene. We found that archaeal diversity in the water column increased with depth and salinity, with 8 OTUs being detected in the epilimnion compared to 21 found in the chemocline, and 32 OTUs in the monimolimnion. Down to 3.5 m depth, the archaeal community was markedly dominated by the presence of an unclassified archaeon sharing 93 % sequence identity to Halogeometricum spp. At the chemocline, the shift in archaeal community composition was associated with an increase in salinity, the main factor affecting the vertical distribution of archaeal assemblages. It appears that the microoxic and hypersaline monimolimnion is populated by several major haloarchaeal taxa, with minor fluctuations in their relative abundances throughout all seasons. The culturable diversity was reasonably correlated to the dominant OTUs obtained by molecular methods. Our results indicate that Ocnei Lake represents a relatively stable extreme habitat, accommodating a diverse and putatively novel archaeal community, as 30 % of OTUs could not be classified at the genus level.

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References

  • Alexe M (2010) Studiul lacurilor sărate din Depresiunea Transilvaniei. Ed. Presa Universitară Clujeană, Cluj Napoca (In Romanian)

  • Alexe M, Furtună P (2012) Natural and anthropic risks in the area of Durgău-Valea Sărată Turda salt lakes. In: Gâştescu P, Lewis W Jr, Breţcan P (eds) Water resources and wetlands. Tulcea, Romania, pp 244–247

    Google Scholar 

  • Alinei R, Ionica A, Cheratoiu C, Cicu A, Gheorghiţa D, Guzu D, Falamas R, Bucurenciu C, Arimie B, Mironescu M, Oprean L (2006) Isolation of halophilic microorganisms in the saline lakes from Ocna Sibiului and anlaysis of red pigments production. Acta Univ Cibiensis E Food Technol 10:21–33

    Google Scholar 

  • Amoozegar MA, Makhdoumi-Kakhki A, Shahzadeh Fazeli SA, Azarbaijani R, Ventosa A (2012) Halopenitus persicus gen. nov., sp. nov., an archaeon from an inland salt lake. Int J Syst Evol Microbiol 62:1932–1936

    Article  CAS  PubMed  Google Scholar 

  • Andrei AŞ, Banciu HL, Oren A (2012) Living with salt: metabolic and phylogenetic diversity of archaea inhabiting saline ecosystems. FEMS Microbiol Lett 330:1–9

    Article  CAS  PubMed  Google Scholar 

  • Antunes A, Taborda M, Huber R, Moissl C, Nobre MF, da Costa MS (2008) Halorhabdus tiamatea sp. nov., a non-pigmented, extremely halophilic archaeon from a deep-sea, hypersaline anoxic basin of the Red Sea, and emended description of the genus Halorhabdus. Int J Syst Evol Microbiol 58:215–220

    Article  CAS  PubMed  Google Scholar 

  • Atlas MR (2004) Handbook of microbiological media, 3rd edn. CRC Press, London

    Book  Google Scholar 

  • Bayly I, Williams WD (1973) Inland waters and their ecology. Longman Australia, Melbourne

    Google Scholar 

  • Benlloch S, López-López A, Casamayor EO, Øvreås L, Goddard V, Daae FL, Smerdon G, Massana R, Joint I, Thingstad F, Pedrós-Alió C, Rodríguez-Valera F (2002) Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ Microbiol 4:349–360

    Article  PubMed  Google Scholar 

  • Boehrer B, Schultze M (2008) Stratification of lakes. Rev Geophys 46: RG2005

  • Borsodi AK, Felföldi T, Máthé I, Bognár V, Knáb M, Krett G, Jurecska L, Tóth EM, Márialigeti K (2013) Phylogenetic diversity of bacterial and archaeal communities inhabiting the saline Lake Red located in Sovata, Romania. Extremophiles 17:87–98

    Article  PubMed  Google Scholar 

  • Bowman JP, McCammon SA, Rea SM, McMeekin TA (2000) The microbial composition of three limnologically disparate hypersaline Antarctic lakes. FEMS Microbiol Lett 183:81–88

    Article  CAS  PubMed  Google Scholar 

  • Bulgăreanu V (1996) Protection and management of anthroposaline lakes in Romania. Lakes Reserv Res Manag 2:211–229

    Article  Google Scholar 

  • Burns DG, Janssen PH, Itoh T, Kamekura M, Echigo A, Dyall-Smith ML (2010) Halonotius pteroides gen. nov., sp. nov., an extremely halophilic archaeon recovered from a saltern crystallizer. Int J Syst Evol Microbiol 60:1196–1199

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265–270

    Google Scholar 

  • Comeau AM, Harding T, Galand PE, Vincent WF, Lovejoy C (2012) Vertical distribution of microbial communities in a perennially stratified Arctic lake with saline, anoxic bottom waters. Sci Rep 2:604

    Article  PubMed Central  PubMed  Google Scholar 

  • Crognale S, Máthé I, Cardone V, Stazi SR, Ráduly B (2013) Halobacterial community analysis of Mierlei saline lake in Transylvania (Romania). Geomicrobiology 30:801–812

    Article  CAS  Google Scholar 

  • Cui HL, Gao X, Yang X, Xu XW (2010a) Halolamina pelagica gen. nov., sp. nov., a new member of the family Halobacteriaceae. Int J Syst Evol Microbiol 61:1617–1621

    Article  PubMed  Google Scholar 

  • Cui HL, Yang X, Gao X, Li XY, Xu XW, Zhou YG, Liu HC, Zhou PJ (2010b) Halogeometricum rufum sp. nov., a halophilic archaeon from a marine solar saltern, and emended description of the genus Halogeometricum. Int J Syst Evol Microbiol 60:2613–2617

    Article  CAS  PubMed  Google Scholar 

  • Cytryn E, Minz D, Oremland RS, Cohen Y (2000) Distribution and diversity of archaea corresponding to the limnological cycle of a hypersaline stratified lake (Solar lake, Sinai, Egypt). Appl Environ Microbiol 66:3269–3276

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Einen J, Thorseth IH, Ovreås L (2008) Enumeration of Archaea and Bacteria in seafloor basalt using real-time quantitative PCR and fluorescence microscopy. FEMS Microbiol Lett 282:182–187

    Article  CAS  PubMed  Google Scholar 

  • Elevi Bardavid R, Khristo P, Oren A (2008) Interrelation between Dunaliella and halophilic prokaryotes in saltern crystallizer ponds. Extremophiles 12:5–14

    Article  PubMed  Google Scholar 

  • Enache M, Itoh T, Kamekura M, Teodosiu G, Dumitru L (2007) Haloferax prahovense sp. nov., an extremely halophilic archaeon isolated from a Romanian salt lake. Int J Syst Evol Microbiol 57:393–397

    Article  CAS  PubMed  Google Scholar 

  • Enache M, Itoh T, Kamekura M, Popescu G, Dumitru L (2008) Halophilic archaea isolated from man-made young (200 years) salt lakes in Slănic, Prahova, Romania. Cent Eur J Biol 3:388–395

    Article  CAS  Google Scholar 

  • Falb M, Müller K, Königsmaier L, Oberwinkler T, Horn P, von Gronau S, Gonzalez O, Pfeiffer F, Bornberg-Bauer E, Oesterhelt D (2008) Metabolism of halophilic archaea. Extremophiles 12:177–196

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan P (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4. http://palaeo-electronica.org/2001_1/past/past.pdf

  • Humayoun SB, Bano N, Hollibaugh JT (2003) Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Appl Environ Microbiol 69:1030–1042

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jiang H, Dong H, Yu B, Liu X, Li Y, Ji S, Zhang CL (2007) Microbial response to salinity change in Lake Chaka, a hypersaline lake on Tibetan plateau. Environ Microbiol 9:2603–2621

    Article  CAS  PubMed  Google Scholar 

  • Keresztes ZG, Felföldi T, Somogyi B, Székely G, Dragos N, Márialigeti K, Bartha C, Vörös L (2012) First record of picophytoplankton diversity in Central European hypersaline lakes. Extremophiles 16:759–769

    Article  PubMed  Google Scholar 

  • La Cono V, La Spada G, Arcadi E, Placenti F, Smedile F, Ruggeri G, Michaud L, Raffa C, De Domenico E, Sprovieri M, Mazzola S, Genovese L, Giuliano L, Slepak VZ, Yakimov MM (2013) Partaking of Archaea to biogeochemical cycling in oxygen-deficient zones of meromictic saline Lake Faro (Messina, Italy). Environ Microbiol 15:1717–1733

    Article  PubMed  Google Scholar 

  • Lane D (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematic. Wiley, New York, pp 115–175

    Google Scholar 

  • Lauro FM, DeMaere MZ, Yau S, Brown MV, Ng C, Wilkins D, Raftery MJ, Gibson JA, Andrews-Pfannkoch C, Lewis M, Hoffman JM, Thomas T, Cavicchioli R (2011) An integrative study of a meromictic lake ecosystem in Antarctica. ISME J 5:879–895

    Article  CAS  PubMed  Google Scholar 

  • Lay CY, Mykytczuk NC, Niederberger TD, Martineau C, Greer CW, Whyte LG (2012) Microbial diversity and activity in hypersaline high Arctic spring channels. Extremophiles 16:177–191

    Article  CAS  PubMed  Google Scholar 

  • Lentini V, Gugliandolo C, Maugeri TL (2012) Vertical distribution of Archaea and Bacteria in a meromictic lake as determined by fluorescent in situ hybridization. Curr Microbiol 64:66–74

    Article  CAS  PubMed  Google Scholar 

  • Makhdoumi-Kakhki A, Amoozegar MA, Bagheri M, Ramezani M, Ventosa A (2012a) Haloarchaeobius iranensis gen. nov., sp. nov., an extremely halophilic archaeon isolated from a saline lake. Int J Syst Evol Microbiol 62:1021–1026

    Article  CAS  PubMed  Google Scholar 

  • Makhdoumi-Kakhki A, Amoozegar MA, Kazemi B, Pašić L, Ventosa A (2012b) Prokaryotic diversity in Aran-Bidgol salt lake, the largest hypersaline playa in Iran. Microbes Environ 27:87–93

    Article  PubMed  Google Scholar 

  • Meuser JE, Baxter BK, Spear JR, Peters JW, Posewitz MC, Boyd ES (2013) Contrasting patterns of community assembly in the stratified water column of Great Salt Lake, Utah. Microb Ecol 66:268–280

    Article  CAS  PubMed  Google Scholar 

  • Muntean V, Crişan D, Kiss S, Drăgan-Bularda M (1996) Enzymological classification of salt lakes in Romania. Int J Salt Lake Res 5:35–44

    Article  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Muyzer G, Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 78:1332–1334

    Google Scholar 

  • Oren A (2001) The bioenergetic basis for the decrease in metabolic diversity at increasing salt concentrations: implications for the functioning of salt lake ecosystems. Hydrobiologia 466:61–72

    Article  CAS  Google Scholar 

  • Oren A (2002) Molecular ecology of extremely halophilic Archaea and Bacteria. FEMS Microbiol Ecol 39:1–7

    CAS  PubMed  Google Scholar 

  • Oren A (2013) Life at high salt and low oxygen: how do the Halobacteriaceae cope with low oxygen concentrations in their environment? Polyextremophiles, vol 27. Springer, Netherlands, pp 531–548

    Chapter  Google Scholar 

  • Oren A, Elevi R, Watanabe S, Ihara K, Corcelli A (2002) Halomicrobium mukohataei gen. nov., comb. nov., and emended description of Halomicrobium mukohataei. Int J Syst Evol Microbiol 52:1831–1835

    Article  CAS  PubMed  Google Scholar 

  • Pagaling E, Wang H, Venables M, Wallace A, Grant WD, Cowan DA, Jones BE, Ma Y, Ventosa A, Heaphy S (2009) Microbial biogeography of six salt lakes in Inner Mongolia, China, and a salt lake in Argentina. Appl Environ Microbiol 75:5750–5760

    CAS  PubMed Central  PubMed  Google Scholar 

  • Podell S, Ugalde JA, Narasingarao P, Banfield JF, Heidelberg KB, Allen EE (2013) Assembly-driven community genomics of a hypersaline microbial ecosystem. PLoS ONE 8:e61692

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Scholten JC, Joye SB, Hollibaugh JT, Murrell JC (2005) Molecular analysis of the sulfate reducing and archaeal community in a meromictic soda lake (Mono Lake, California) by targeting 16S rRNA, mcrA, apsA, and dsrAB genes. Microb Ecol 50:29–39

    Article  CAS  PubMed  Google Scholar 

  • Shannon C, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Champaign

    Google Scholar 

  • Swan BK, Ehrhardt CJ, Reifel KM, Moreno LI, Valentine DL (2010) Archaeal and bacterial communities respond differently to environmental gradients in anoxic sediments of a California hypersaline lake, the Salton Sea. Appl Environ Microbiol 76:757–768

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci USA 108:8420–8425

    Article  CAS  PubMed  Google Scholar 

  • Wainø M, Tindall BJ, Ingvorsen K (2000) Halorhabdus utahensis gen. nov., sp. nov., an aerobic, extremely halophilic member of the Archaea from Great Salt Lake, Utah. Int J Syst Evol Microbiol 50:183–190

    Article  PubMed  Google Scholar 

  • Yanan Y, Breitbart M, McNairnie P, Rohwer F (2006) FastGroupII: A web-based bioinformatics platform for analyses of large 16S rDNA libraries. BMC Bioinformatics 7

  • Youssef NH, Ashlock-Savage KN, Elshahed MS (2012) Phylogenetic diversities and community structure of members of the extremely halophilic Archaea (order Halobacteriales) in multiple saline sediment habitats. Appl Environ Microbiol 78:1332–1344

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants of the Romanian National Authority for Scientific Research, CNCS–UEFIS-CDI, project numbers PN-II-ID-PCE-2011-3-0546 and PN-II-ID-PCE-2011-3-0765. We thank Dr. Cosmin Sicora for technical support in qPCR analysis. We are grateful to Dr. Ovidiu Mera for the permission to enter the study area, and to Prof. Elena Rakosy and Prof. Constantin Crăciun for their consent to use the microscopy facilities.

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Correspondence to Horia Leonard Banciu.

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Communicated by A. Oren.

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Baricz, A., Coman, C., Andrei, A.Ş. et al. Spatial and temporal distribution of archaeal diversity in meromictic, hypersaline Ocnei Lake (Transylvanian Basin, Romania). Extremophiles 18, 399–413 (2014). https://doi.org/10.1007/s00792-013-0625-6

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