Skip to main content

Advertisement

SpringerLink
Log in

Microbial Composition and Diversity Patterns in Deep Hyperthermal Aquifers from the Western Plain of Romania

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

A limited number of studies have investigated the biodiversity in deep continental hyperthermal aquifers and its influencing factors. Here, we present the first description of microbial communities inhabiting the Pannonian and Triassic hyperthermal aquifers from the Western Plain of Romania, the first one being considered a deposit of “fossilized waters,” while the latter is embedded in the hydrological cycle due to natural refilling. The 11 investigated drillings have an open interval between 952 and 3432 m below the surface, with collected water temperatures ranging between 47 and 104 °C, these being the first microbial communities characterized in deep continental water deposits with outflow temperatures exceeding 80 °C. The abundances of bacterial 16S rRNA genes varied from approximately 105–106 mL−1 in the Pannonian to about 102–104 mL−1 in the Triassic aquifer. A 16S rRNA gene metabarcoding analysis revealed distinct microbial communities in the two water deposits, especially in the rare taxa composition. The Pannonian aquifer was dominated by the bacterial genera Hydrogenophilus and Thermodesulfobacterium, together with archaeal methanogens from the Methanosaeta and Methanothermobacter groups. Firmicutes was prevalent in the Triassic deposit with a large number of OTUs affiliated to Thermoanaerobacteriaceae, Thermacetogenium, and Desulfotomaculum. Species richness, evenness, and phylogenetic diversity increased alongside with the abundance of mesophiles, their presence in the Triassic aquifer being most probably caused by the refilling with large quantities of meteoric water in the Carpathian Mountains. Altogether, our results show that the particular physico-cheminal characteristics of each aquifer, together with the water refilling possibilities, seem to determine the microbial community structure.

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

Similar content being viewed by others

References

  1. Nyyssönen M, Bomberg M, Kapanen A, Nousiainen A, Pitkänen P, Itävaara M (2012) Methanogenic and sulphate-reducing microbial communities in deep groundwater of crystalline rock fractures in Olkiluoto, Finland Geomicrobiol J. 29:863–878. doi:10.1080/014904512011635759

    Article  Google Scholar 

  2. Inagaki F, Nunoura T, Nakagawa S, Teske A, Lever M, Lauer A, et al. (2006) Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean margin Proc Nat Acad Sci USA 103:2815–2820

    Article  PubMed  CAS  Google Scholar 

  3. Ragon M, Van-Driessche AES, García-Ruíz JM, Moreira D, Lopez-Garcia P (2013) Microbial diversity in the deep-subsurface hydrothermal aquifer feeding the giant gypsum crystal-bearing Naica Mine, Mexico Front. Microbiol. 4:37. doi:10.3389/fmicb201300037

    Article  PubMed  PubMed Central  Google Scholar 

  4. Walsh EA, Birkpatrick JB, Rutherford SD, Smith DC, Sogin M, Hondt S (2016) Bacterial diversity and community composition from seasurface to subseafloor ISME J 10:979–989

    Article  PubMed  Google Scholar 

  5. Marteinsson VT, Hauksdóttir S, Hobel CFV, Kristmannsdóttir H, Hreggvidsson GO, Kristjánsson JK (2001) Phylogenetic diversity analysis of subterranean hot springs in Iceland Appl. Environ. Microbiol. 67:4242–4248

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Summit M, Baross JA (2001) A novel microbial habitat in the mid-ocean ridge subseafloor Proc. Natl. Acad. Sci. U. S. A. 98:2158–2163

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Kimura H, Asada R, Masta A, Naganuma T (2003) Distribution of microorganisms in the subsurface of the Manus Basin hydrothermal vent field in Papua New Guinea Appl. Environ. Microbiol. 69:644–648. doi:10.1128/AEM691644-6482003

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Hubalek V, Wu X, Eiler A, Buck M, Heim C, Dopson M, et al. (2016) Connectivity to the surface determines diversity patterns in subsurface aquifers of the Fennoscandian shield ISME J 10:2556. doi:10.1038/ismej201636

    Article  PubMed  PubMed Central  Google Scholar 

  9. Sahl JW, Schmidt R, Swanner ED, Mandernack KW, Templeton AS, Kieft TL, et al. (2008) Subsurface microbial diversity in deep-granitic-fracture water in Colorado Appl. Environ. Microbiol. 74:143–152. doi:10.1128/AEM01133-07

    Article  PubMed  CAS  Google Scholar 

  10. Kimura H, Sugihara M, Yamamoto H, Patel BK, Kato K, Hanada S (2005) Microbial community in a geothermal aquifer associated with the subsurface of the Great Artesian Basin, Australia Extremophiles 9: 407–414. doi:10.1007/s00792–005–0454-3

  11. Kieft TL (2016) Microbiology of the Deep Continental Biosphere in Hurst CJ (ed) Their world: A diversity of microbial environments, Springer, Cham pp 225–249

  12. Nyyssönen M, Hultman J, Ahonen L, Kukkonen I, Paulin L, Laine P, et al. (2014) Taxonomically and functionally diverse microbial communities in deep crystalline rocks of the Fennoscandian shield ISME J 8:126–138. doi:10.1038/ismej2013125

    Article  PubMed  Google Scholar 

  13. Lau MC, Cameron C, Magnabosco C, Brown CT, Schilkey F, Grim, et al. (2014) Phylogeny and phylogeography of functional genes shared among seven terrestrial subsurface metagenomes reveal N-cycling and microbial evolutionary relationships Front Microbiol 5:531. doi:10.3389/fmicb201400531

    Article  PubMed  PubMed Central  Google Scholar 

  14. Sogin ML, Morrison HG, Huber JA, Mark-Welch D, Huse SM, Neal PR, et al. (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere” Proc. Natl. Acad. Sci. U. S. A. 103:12115–12120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Brazelton WJ, Nelson B, Schrenk MO (2012) Metagenomic evidence for H 2 oxidation and H 2 production by serpentinite-hosted subsurface microbial communities Front. Microbiol. 2:268. doi:10.3389/fmicb201100268

    Article  PubMed  PubMed Central  Google Scholar 

  16. Chapelle FH, O’Neill K, Bradley PM, Methé BA, Ciufo SA, et al. (2002) A hydrogen-based subsurface microbial community dominated by methanogens Nature 415:312–315. doi:10.1038/415312a

    Article  PubMed  Google Scholar 

  17. Lin LH, Wang PL, Rumble D, Lippmann-Pipke J, Boice E, Pratt LM, et al. (2006) Long term biosustainability in a high energy, low diversity crustal biotome Science 314:479

    Article  PubMed  CAS  Google Scholar 

  18. Roussel EG, Bonavita MA, Querellou J, Cragg BA, Webster G, Prieur D, et al. (2008) Extending the sub-sea-floor biosphere Science 320:1046

    Article  PubMed  CAS  Google Scholar 

  19. Hengsuwan M, Heim C, Simon K, Hansen BT (2015) Long-term investigation of Sr-isotope and rare earth element fractionation processes within three major aquifers in the Äspö hard rock laboratory (Sweden) Geomicrobial J 32:243–254

    Article  CAS  Google Scholar 

  20. Țenu A (1981) Zăcăminte de ape hipertermale din Nord-Vestul României. Editura Academiei Republicii Socialiste România, București,

    Google Scholar 

  21. Bendea C, Bendea G, Rosca M, Cucueteanu D (2013) Current status of geothermal energy production and utilization in Romania J Sustain Energy 4:1–9

    Google Scholar 

  22. Edwards KJ, Becker K, Colwell F (2012) The deep, dark energy biosphere: intraterrestrial life on Earth Annu. Rev. Earth Planet. Sci. 40:551–568

    Article  CAS  Google Scholar 

  23. Lovley DR, Chapelle FH (1995) Deep subsurface microbial precesses Rev. Geophys. 33:365–381

    Article  Google Scholar 

  24. Suenaga E, Nakamura H (2005) Evaluation of three methods for effective extraction of DNA from human hair J Chromatogr B Analyt Technol Biomed Life Sci 820:137–141. doi:10.1016/jjchromb200411028

    Article  PubMed  CAS  Google Scholar 

  25. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley and Sons, Chichester, pp. 115–175

    Google Scholar 

  26. Suzuki M, Taylor L, DeLong E (2006) Quantitative analysis of small subunit rRNA genes in mixed microbial populations via 5′-nuclease assays Appl. Environ. Microbiol. 66:4605–4614

    Article  Google Scholar 

  27. Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction Biotechnol. Bioeng. 89:670–679

    Article  PubMed  CAS  Google Scholar 

  28. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool J. Mol. Biol. 215:403–410

    Article  PubMed  CAS  Google Scholar 

  29. Benson DA, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2015) GenBank Nucleic Acids Res. 43:D30–D35. doi:10.1093/nar/gku1216

    Article  PubMed  CAS  Google Scholar 

  30. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. (2010) QIIME allows analysis of high-throughput community sequencing data Nat. Methods 7:335–336. doi:10.1038/nmethf303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461

    Article  PubMed  CAS  Google Scholar 

  32. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie LE, Keller K, et al. (2006) Greengenes, a chimera-checked 16S rRNA gene database and worlbench compatible with ARB Appl. Environ. Microbiol. 72(7):5069–5072

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. McDonald D, Clemente JC, Kuczynski J, Rideout JR, Stombaugh J, Wendel D, et al. (2012) The biological observation matrix (BIOM) format or: how I learned to stop worrying and love the ome-ome GigaScience 1:–7. doi:10.1186/2047-217X-1-7

  34. Lin X, Kennedy D, Fredrickson J, Bjornstad B, Konopka A (2012) Vertical stratification of subsurface microbial community composition across geological formations at the Hanford site: Hanford site subsurface microbial communities Environ. Microbiol. 14:414–425. doi:10.1111/j1462-2920201102659x

    Article  PubMed  CAS  Google Scholar 

  35. Legendre P, Fortin MJ (2010) Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data Mol. Ecol. Resour. 10:831–844. doi:10.1111/j1755-0998201002866x

    Article  PubMed  Google Scholar 

  36. Galtier N, Lobry JR (1997) Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes J. Mol. Evol. 44:632–636

    Article  PubMed  CAS  Google Scholar 

  37. Kimura H, Ishibashi JI, Masuda H, Kato K, Hanada S (2007) Selective phylogenetic analysis (SePA) targeting 16S rRNA gene of hyperthermophilic archaea in the deep-subsurface hot biosphere Appl. Environ. Microbiol. 73:2110–2117. doi:10.1128/AEM02800-06

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Agarwala R, Barrett T, Beck J, Benson DA (2016) Database resources of the National Center for biotechnology information Nucleic Acids Res. 44:D7-19. doi:10.1093/nar/gkv1290

    Article  CAS  Google Scholar 

  39. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences Nat. Biotechnol.:8, 1–10. doi:10.1038/nbt2676

  40. Kovácz J, Balázs I, Jákfalvi S (2013) Studiul forajelor geotermale. Program de cercetare în Euroregiunea Hajdú-Bihar – Bihor pentru cunoaşterea stării hidrogeologice a corpurilor de apă termală transfrontaliere. Proiect finanţat prin programul de Cooperare Transfrontalieră Ungaria - România 2007–2013

  41. Itävaara M, Nyyssönen M, Kapanen A, Nousiainen A, Ahonen L, Kukkonen I (2011) Characterization of bacterial diversity to a depth of 1500 m in the Outokumpu Deep Borehole, Fennoscandian shield: deep terrestrial biodiversity FEMS Microbiol. Ecol. 77:295–309. doi:10.1111/j1574-6941201101111x

    Article  PubMed  Google Scholar 

  42. Purkamo L, Bomberg M, Kietäväinen R, Salavirta H, Nyyssönen M, Nuppunen-Puputti M, et al. (2016) Microbial co-occurrence patterns in deep Precambrian bedrock fracture fluids Biogeosciences 13:3091–3108. doi:10.5194/bg-13-3091-2016

    Article  Google Scholar 

  43. Onstott TC, Lin LH, Davidson M, Mislowack B, Borcsik M, Hall J, et al. (2006) The origin and age of biogeochemical trends in deep fracture water of the Witwatersrand Basin, South Africa Geomicrobiol J. 23:369–414. doi:10.1080/01490450600875688

    Article  CAS  Google Scholar 

  44. Moser DP, Onstott TC, Fredrickson JK, Brockman FJ, Balkwill DL, Drake GR, et al. (2003) Temporal shifts in the geochemistry and microbial community structure of an ultradeep mine borehole following isolation Geomicrobiol J. 20:517–548. doi:10.1080/713851170

    Article  CAS  Google Scholar 

  45. Gihring TM, Moser DP, Lin LH, Davidson M, Onstott TC, Morgan L, et al. (2006) The distribution of microbial taxa in the subsurface water of the Kalahari shield, South Africa Geomicrobiol J. 23:415–430 doi:10.1080/01490450600875696

    Article  CAS  Google Scholar 

  46. Oren A (2014) The Family Methanobacteriaceae in Rosenberg E, DeLong EF, Lory S, et al (eds) The Prokaryotes, Springer, Berlin, Heidelberg pp 165–193

  47. Oren A (2014) The Family Rhodocyclaceae. In: Rosenberg E, EF DL, Lory S, et al. (eds) The Prokaryotes. Springer, Berlin, pp. 975–998

    Chapter  Google Scholar 

  48. Hayashi NR, Ishida T, Yokota A, Kodama T, Igarashi Y (1999) Hydrogenophilus thermoluteolus gen nov, sp nov, a thermophilic, facultatively chemolithoautotrophic, hydrogen-oxidizing bacterium Int J Syst Evol Micr 49:783–786

    Google Scholar 

  49. Vesteinsdottir H, Reynisdottir DB, Orlygsson J (2011) Hydrogenophilus islandicus sp nov, a thermophilic hydrogen-oxidizing bacterium isolated from an Icelandic hot spring Intl J Syst Evol Micr 61:290–294. doi:10.1099/ijs0023572-0

    Article  CAS  Google Scholar 

  50. Stöhr R, Waberski A, Liesack W, Völker H, Wehmeyer U, Thomm M (2001) Hydrogenophilus hirschii sp nov, a novel thermophilic hydrogen-oxidizing Beta-Proteobacterium isolated from Yellowstone national park Intl J Syst Evol Micr 51:481–488. doi:10.1099/00207713-51-2-481

    Article  Google Scholar 

  51. Bhatnagar S, Badger JH, Madupu R, Khouri HM, O’Connor EM, Robb FT, et al. (2015) Genome sequence of a sulfate-reducing thermophilic bacterium, Thermodesulfobacterium commune DSM 2178T (phylum Thermodesulfobacteria) Genome Announc 3:e01490–e01414. doi:10.1128/genomeA01490-14

    Article  PubMed  PubMed Central  Google Scholar 

  52. Pham VD, Hnatow LL, Zhang S, Fallon RD, Jackson SC, Tomb JF, et al. (2009) Characterizing microbial diversity in production water from an Alaskan mesothermic petroleum reservoir with two independent molecular methods Environ. Microbiol. 11:176–187. doi:10.1111/j1462-2920200801751x

    Article  PubMed  CAS  Google Scholar 

  53. Dong Y, Kumar CG, Chia N, Kim PJ, Miller PA, Price ND, et al. (2014) Halomonas sulfidaeris - dominated microbial community inhabits a 18 km-deep subsurface Cambrian sandstone reservoir Environ. Microbiol. 16:1695–1708. doi:10.1111/1462–292012325

    Article  PubMed  CAS  Google Scholar 

  54. Davidson MM, Silver BJ, Onstott TC, Moser DP, Gihring TH, Pratt LM, et al. (2011) Capture of planktonic microbial diversity in fractures by long-term monitoring of flowing boreholes, Evander Basin, South Africa Geomicrobiol J. 28:275–300. doi:10.1080/014904512010499928

    Article  Google Scholar 

  55. Aüllo T, Ranchou-Peyruse A, Ollivier B, Magot M (2013) Desulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environments Front. Microbiol. 4:362. doi:10.3389/fmicb201300362

    Article  PubMed  PubMed Central  Google Scholar 

  56. Mladenovska Z, Mathrani IM (1995) Ahring, BK Isolation and characterization of Caldicellulosiruptor lactoaceticus sp nov, an extremely thermophilic, cellulolytic, anaerobic bacterium. Arch. Microbiol. 163: 223–230. doi:10.1007/BF00305357

    Article  CAS  Google Scholar 

  57. Huang CY, Patel BK, Mah RA, Baresi L (1998) Caldicellulosiruptor owensensis sp nov, an anaerobic, extremely thermophilic, xylanolytic bacterium Intl J Syst Evol Micr 48:91–97

    Google Scholar 

  58. Miroshnichenko ML, Kublanov IV, Kostrikina NA, Tourova TP, Kolganova TV, Birkeland NK, et al. (2008) Caldicellulosiruptor kronotskyensis sp. nov. and Caldicellulosiruptor hydrothermalis sp. nov., two extremely thermophilic, cellulolytic, anaerobic bacteria from Kamchatka thermal springs Intl J Syst Evol Micr 58:1492–1496. doi:10.1099/ijs065236-0

    Article  CAS  Google Scholar 

  59. Widdel F (2006) The Genus Desulfotomaculum. In: Dworkin M, Falkow S, Rosenberg E (eds) The Prokaryotes. Springer, New York, pp. 787–794

    Chapter  Google Scholar 

  60. Nazina TN, Ivanova AE, Kanchaveli LP, Rozanova EP (1989) A new sporeforming thermophilic methylotrophic sulfate-reducing bacterium, Desulfotomaculum kutznetsovii sp. nov Mikrobiologiya (Translated) 57:823–827

    Google Scholar 

  61. O’Sullivan LA, Roussel EG, Weightman AJ, Webster G, Hubert CRJ, Bell E (2015) Survival of Desulfotomaculum spores form estuarine sediments after serial autoclaving and hith-temperature exposure ISME J 9:922–933

    Article  PubMed  CAS  Google Scholar 

  62. Zillig W, Holz I, Janekovic D, Schifer W, Reiter WD (1983) The archaebacterium Thermococcus celer represents, a novel genus within the thermophilic branch of the archaebacteria System Appl Microbiol 4:88–94

    Article  CAS  Google Scholar 

  63. Huber H, Huber R, Steter KO (2006) Thermoproteales. In: Dworkin M, Falkow S, Rosenberg E (eds) The Prokaryotes. Springer, New York, pp. 10–22

    Chapter  Google Scholar 

  64. Hartzell P, Reed DW (2006) The Genus Archaeoglobus. In: Dworkin M, Falkow S, Rosenberg E (eds) The Prokaryotes. Springer, New York, pp. 82–100

    Chapter  Google Scholar 

  65. Palleroni NJ, Bradbury JF (1993) Stenotrophomonas, a new bacterial genus for Xanthomonas maltophilia (Hugh 1980) Swings et al 1983 Intl J Syst Evol Micr 43:606–609. doi:10.1099/00207713–43–3-606

    Article  CAS  Google Scholar 

  66. Borsodi AK, Szirányi B, Krett G, Márialigeti K, Janurik E, Pekár F (2016) Changes in the water quality and bacterial community composition of an alkaline and saline oxbow lake used for temporary reservoir of geothermal waters Environ. Sci. Pollut. Res. 23:17676. doi:10.1007/s11356-016-6923-7

    Article  CAS  Google Scholar 

  67. Cheng L, Shi S, Li Q, Chen J, Zhang H, Lu Y (2014) Progressive degradation of crude oil n-Alkanes coupled to methane production under mesophilic and thermophilic conditions PLoS ONE 9:e113253. doi:10.1371/journalpone0113253

    Article  PubMed  PubMed Central  Google Scholar 

  68. Fang HHP, Liang DW, Zhang T, Liu Y (2006) Anaerobic treatment of phenol in wastewater under thermophilic condition Water Res. 40:427–434. doi:10.1016/jwatres200511025

    Article  PubMed  CAS  Google Scholar 

  69. Lladser ME, Gouet R, Reeder J (2011) Extrapolation of Urn models via poissonization: accurate measurements of the microbial unknown PLoS One 6:e21105. doi:10.1371/journalpone0021105

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Inskeep WP, Rusch DB, Jay ZJ, Herrgard MJ, Kozubal MA, Richardson TH, et al. (2010) Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function PLoS One 5:e9773. doi:10.1371/journalpone0009773

    Article  PubMed  PubMed Central  Google Scholar 

  71. Sharp CE, Brady AL, Sharp GH, Grasby SE, Stott MB, Dunfield PF (2014) Humboldt’s spa: microbial diversity is controlled by temperature in geothermal environments ISME J 8:1166–1174

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Lau CY, Jing HM, Aitchison JC, Pointing SB (2006) Highly diverse community structure in a remote central Tibetan geothermal spring does not display monotonic variation to thermal stress FEMS Microbiol. Ecol. 57(1):80–91. doi:10.1111/j1574-6941200600104x

    Article  Google Scholar 

  73. Purcell D, Sompong U, Lau CY, Barraclough TG, Peerapornpisal Y, Pointing SB (2007) The effects of temperature, pH and sulphide on the community structure of Hyperthermophilic streamers in Hot Springs of northern Thailand FEMS Microbiol. Ecol. 60(3):456–466. doi:10.1111/j1574-6941200700302x

    Article  PubMed  CAS  Google Scholar 

  74. Wang S, Weiguo H, Hailiang D, Hongchen J, Liuqin H, Geng W, Chuanlun Z, et al. (2013) Control of temperature on microbial community structure in Hot Springs of the Tibetan plateau PLoS One 8(5):e62901. doi:10.1371/journalpone0062901

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Meyer-Dombard DR, Amend JP (2014) Geochemistry and microbial ecology in alkaline hot springs of Ambitle Island, Papua New Guinea Extremophiles 18:763. doi:10.1007/s00792-014-0657-6

    Article  PubMed  CAS  Google Scholar 

  76. Headd B, Engel AS (2014) Biogeographic congruency among bacterial communities from terrestrial sulfidic springs Front. Microbiol. 5:473. doi:10.3389/fmicb201400473

    Article  PubMed  PubMed Central  Google Scholar 

  77. Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities Appl. Environ. Microbiol. 73:1576–1585. doi:10.1128/AEM01996-06

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Bomberg M, Lamminmäki T, Itävaara M (2016) Microbial communities and their predicted metabolic characteristics in deep fracture groundwaters of the crystalline bedrock of Olkiluoto, Finland Biogeosciences 13:6031–6047. doi:10.5194/bg-13-6031-2016

    Article  CAS  Google Scholar 

  79. Kamagata Y, Kawasaki H, Oyaizu H, Nakamura K, Mikami E, Endo G, Koga Y, Yamasato K (1992) Characterization of three thermophilic strains of Methanothrix (“Methanosaeta”) thermophila sp nov and rejection of Methanothrix (“Methanosaeta”) thermoacetophila Int. J. Syst. Bacteriol. 42:463–468

    Article  PubMed  CAS  Google Scholar 

  80. Wasserfallen A, Nölling J, Pfister P, Reeve J, Conway de Macario E (2000) Phylogenetic analysis of 18 thermophilic Methanobacterium isolates supports the proposals to create a new genus, Methanothermobacter gen. nov., and to reclassify several isolates in three species, Methanothermobacter thermautotrophicus comb. nov., Methanothermobacter wolfeii comb. nov., and Methanothermobacter marburgensis sp. nov Intl J Syst Evol Mic 50:43–53

    Article  CAS  Google Scholar 

  81. Oremland RS, Polcin S (1982) Methanogenesis and sulfate reduction: competitive and noncompetitive substrates in estuarine sediments Appl. Environ. Microbiol. 44:1270–1276

    PubMed  PubMed Central  CAS  Google Scholar 

  82. Berg IA (2011) Ecological aspects of the distribution of different autotrophic CO2 fixation pathways Appl. Environ. Microbiol. 77:1925–1936

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Campbell BJ, Cary C (2004) Abundance of reverse tricarboxylic acid cycle genes in free-living microorganisms at deep-sea hydrothermal vents Appl. Environ. Microbiol. 70:6282–6289. doi:10.1128/AEM70106282-62892014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Magnabosco C, Ryan K, Lau MC, Kuloyo O, Lollar BS, Kieft TL, van Heerden E, Onstott TC (2016) A metagenomic window into carbon metabolism at 3 km depth in Precambrian continental crust ISME J 10:730–741

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was partially supported by the EnviroAMR project (grant no. 3499/20.05.2015, financed through the EEA 2009-2014 Financial Mechanism) through the EnviroBioInfo bioinformatic center. CMC and ES were also supported by the POSDRU/187/1.5/S/155383 research scholarship programme. All the samples were collected with the approval of S.C. TRANSGEX S.A. company. The authors wish to thank Dr. Codruta Bendea (University of Oradea) and Sanda Sferle (TRANSGEX) for their valuable support towards obtaining the water samples.

Author information

Authors and Affiliations

  1. NIRDBS, Institute of Biological Research, 48 Republicii street, 400015, Cluj-Napoca, Romania

    Cecilia M. Chiriac, Andreea Baricz, Edina Szekeres, Nicolae Dragoș & Cristian Coman

  2. Molecular Biology and Biotechnology Department, Faculty of Biology and Geology, Babeş-Bolyai University, Cluj-Napoca, Romania

    Cecilia M. Chiriac, Andreea Baricz, Edina Szekeres & Nicolae Dragoș

  3. Chemistry, Biotechnology and Food Science Department, Norwegian University of Life Sciences, Aas, Norway

    Knut Rudi

Authors
  1. Cecilia M. Chiriac
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andreea Baricz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edina Szekeres
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Knut Rudi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nicolae Dragoș
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cristian Coman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cristian Coman.

Electronic supplementary materials

ESM 1

(Zip 564 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chiriac, C.M., Baricz, A., Szekeres, E. et al. Microbial Composition and Diversity Patterns in Deep Hyperthermal Aquifers from the Western Plain of Romania. Microb Ecol 75, 38–51 (2018). https://doi.org/10.1007/s00248-017-1031-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-1031-x

Keywords

Search

Navigation