Advertisement

Microbial Ecology

, Volume 69, Issue 2, pp 293–306 | Cite as

Microbiology of Healing Mud (Fango) from Roman Thermae Aquae Iasae Archaeological Site (Varaždinske Toplice, Croatia)

  • Janez Mulec
  • Václav Krištůfek
  • Alica Chroňáková
  • Andreea Oarga
  • Josef Scharfen
  • Martina Šestauberová
Environmental Microbiology

Abstract

We found well-preserved, rocky artefacts that had been buried in the healing mud (fango) for more than 1,500 years at the Roman archaeological site at Varaždinske Toplice. This Roman pool with fango sediments and artefacts is fed from hot sulphidic springs. The fango exhibited nearly neutral pH, a high level of organic C, an elevated concentration of heavy metals and a high total microbial biomass, greater than 108 cells per gram of dry weight. The dominant microbes, assessed by molecular profiling (denaturing gradient gel electrophoresis), were affiliated with Thiobacillus, Sulfuricurvum, Polaromonas, and Bdellovibrio. Polymerase chain reaction screening for microbial functional guilds revealed the presence of sulphur oxidizers and methanogens but no sulphate reducers. The dominance of four Proteobacterial classes (α-, β-, δ- and ε-Proteobacteria) was confirmed by fluorescence in situ hybridisation; Actinobacteria were less abundant. Cultivable bacteria represented up to 23.4 % of the total bacterial counts when cultivation media was enriched with fango. These bacteria represented the genera Acinetobacter, Aeromonas, Arthrobacter, Comamonas, Ewingella, Flavobacterium, Pseudomonas, Rahnella and Staphylococcus. This study showed that the heterogeneous nature of fango at neutral pH created various microniches, which largely supported microbial life based on sulphur-driven, autotrophic denitrification.

Keywords

Thiobacillus Archaeological Artefact Anaerobic Methane Oxidation Polaromonas Total Microbial Count 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The study was partly supported by the Slovenian Research Agency (J6-0152, P6-0119 and L1-5453) and the inter-academic exchange program between the Czech Academy of Sciences and the Slovenian Academy of Sciences and Arts. The authors are particularly grateful to Spomenka Vlahović and Hrvoje Posilović for assistance and excellent cooperation during the archaeological excavation; to Franjo Drole for assistance during field work; and to Boštjan Geohelli for the facility support. The authors also thank the Laboratory of Electron Microscopy–Institute of Parasitology BC AS CR, v. v. i. in České Budějovice for a productive collaboration on scanning electron microscopy. Finally, the authors would like to thank Majka Stehlíková and Mateja Zadel for laboratory assistance and San Francisco Edit for language assistance.

References

  1. 1.
    Zolitschka B, Anselmetti F, Ariztegui D, Corbella H, Francus P, Lucke A, Maidana N, Ohlendorf C, Schabitz F, Wastegard S (2013) Environment and climate of the last 51,000 years—new insights from the Potrok Aike maar lake Sediment Archive Drilling prOject (PASADO). Quat Sci Rev 71:1–12. doi: 10.1016/j.quascirev.2012.11.024 CrossRefGoogle Scholar
  2. 2.
    Santiago-Rodriguez T, Narganes-Storde Y, Chanlatte L, Crespo-Torres E, Toranzos G, Jimenez-Flores R, Hamrick A, Cano R (2013) Microbial communities in pre-Columbian coprolites. Plos One 8. doi:  10.1371/journal.pone.0065191
  3. 3.
    Dutour O (2008) Archaeology of human pathogens: palaeopathological appraisal of palaeoepidemiology. In: Raoult D, Drancourt M (eds) Paleomicrobiology. Springer, Berlin, pp 125–144CrossRefGoogle Scholar
  4. 4.
    Bader NA, Al-Gharib WK (2013) Restoration and preservation of engraved limestone blocks discovered in Abu Mousa excavation, Suez-Egypt. Int J Conserv Sci 4:25–42Google Scholar
  5. 5.
    Vlahović S (2012) Overview of conservation and restoration works on the Newly-discovered Roman relief with a three-nymph motif from Varaždinske Toplice, preliminary communication. Radovi Zavoda za znanstveni rad HANU Varaždin 23:301–309Google Scholar
  6. 6.
    Pfeifruck J (2008) Roman marble relief with nymph representation from local museum Varaždinske Toplice (Croatia)—documentation of conservation and restoration work on the relief with nymph presentation [in German]. Zavičajni muzej Varaždinske Toplice, Varaždinske TopliceGoogle Scholar
  7. 7.
    Tiano P (2002) Biodegradation of cultural heritage: decay mechanisms and control methods. In: Proceedings ARIADNE Workshop 9—historic materials and their diagnostics, Department of Conservation and Restoration, New University of Lisbon, Lisbon, pp 7–12Google Scholar
  8. 8.
    Enning D, Garrelfs J (2014) Corrosion of iron by sulfate-reducing bacteria: new views of an old problem. Appl Environ Microb 80:1226–1236CrossRefGoogle Scholar
  9. 9.
    De Belie N (2010) Microorganisms versus stony materials: a love–hate relationship. Mater Struct 43:1191–1202. doi: 10.1617/s11527-010-9654-0 CrossRefGoogle Scholar
  10. 10.
    Videla H (2001) Microbially induced corrosion: an updated overview (reprinted). Int Biodeter Biodegr 48:176–201. doi: 10.1016/S0964-8305(01)00081-6 CrossRefGoogle Scholar
  11. 11.
    Šimunić A, Avanić R (2008) Varaždinske Toplice [in Croatian]. In: Šimunić A (ed) Geothermal and mineral waters of the Republic of Croatia (geologic monograph), Hrvatski Geološki Institut, Zagreb, pp 205–217Google Scholar
  12. 12.
    Miholić S (1954) History of mineral waters in Croatia [in Croatian]. In: Grmek MD, Dujmušić S (eds) From Croatian medical history. Zbor liječnika Hrvatske, Zagreb, pp 107–113Google Scholar
  13. 13.
    Vlahović S (2009) Historical analyses of sulfur thermomineral water in Varaždinske Toplice based on the library fund of the regional museum in Varaždinske Toplice [in Croatian]. In: Ivanišević G (ed) 300 years of balneological analyses in Croatia. Akademija medicinskih znanosti Hrvatske, Zagreb, pp 84–91Google Scholar
  14. 14.
    Ivanišević G (2009) Croatian thermomineral waters [in Croatian]. In: Ivanišević G (ed) 300 years of balneological analyses in Croatia. Akademija medicinskih znanosti Hrvatske, Zagreb, pp 51–64Google Scholar
  15. 15.
    Barić L (1963) Sulfur from Varaždinske Toplice in Croatia [in Croatian]. Geol Vjesn 16:13–20Google Scholar
  16. 16.
    Tomić D (1947) The content of fluorine in thermal sulfur water of Ilidže at Sarajevo and Varaždinske Toplice [in Croatian]. Farmaceut Glasn 3:129–131Google Scholar
  17. 17.
    Clesceri LS, Greenberg AE, Eaton AD (1998) Standard methods for the examination of water and wastewater. American Public Health Association, WashingtonGoogle Scholar
  18. 18.
    Zbíral J (1995) Soil analyses, part 1 (in Czech). Central Institute for Supervising and Testing in Agriculture, BrnoGoogle Scholar
  19. 19.
    Krištůfek V, Elhottová D, Chroňáková A, Dostálková I, Picek T, Kalčík J (2005) Growth strategy of heterotrophic bacterial population along successional sequence on spoil of brown coal colliery substrate. Folia Microbiol 50:427–435. doi: 10.1007/BF02931425 CrossRefGoogle Scholar
  20. 20.
    Seng P, Drancourt M, Gouriet F, La Scola B, Fournier PE, Rolain JM, Raoult D (2009) Ongoing revolution in bacteriology: routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clin Infect Dis 49:543–551. doi: 10.1086/600885 PubMedCrossRefGoogle Scholar
  21. 21.
    Brons J, van Elsas J (2008) Analysis of bacterial communities in soil by use of denaturing gradient gel electrophoresis and clone libraries, as influenced by different reverse primers. Appl Environ Microb 74:2717–2727. doi: 10.1128/AEM.02195-07 CrossRefGoogle Scholar
  22. 22.
    Chroňáková A, Ascher J, Jirout J, Ceccherini M, Elhottová D, Pietramellara G, Šimek M (2013) Cattle impact on composition of archaeal, bacterial, and fungal communities by comparative fingerprinting of total and extracellular DNA. Biol Fert Soils 49:351–361. doi: 10.1007/s00374-012-0726-x CrossRefGoogle Scholar
  23. 23.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids S 41:95–98Google Scholar
  24. 24.
    Kim O, Cho Y, Lee K, Yoon S, Kim M, Na H, Park S, Jeon Y, Lee J, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. IJSEM 62:716–721. doi: 10.1099/ijs.0.038075-0 PubMedGoogle Scholar
  25. 25.
    Luton P, Wayne J, Sharp R, Riley P (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiol-Sgm 148:3521–3530Google Scholar
  26. 26.
    Kondo R, Nedwell D, Purdy K, Silva S (2004) Detection and enumeration of sulphate-reducing bacteria in estuarine sediments by competitive PCR. Geomicrobiol J 21:145–157. doi: 10.1080/01490450490275307 CrossRefGoogle Scholar
  27. 27.
    Petri R, Podgorsek L, Imhoff J (2001) Phylogeny and distribution of the soxB gene among thiosulfate-oxidizing bacteria. FEMS Microbiol Lett 197:171–178. doi: 10.1111/j.1574-6968.2001.tb10600.x PubMedCrossRefGoogle Scholar
  28. 28.
    Rother D, Henrich H, Quentmeier A, Bardischewsky F, Friedrich C (2001) Novel genes of the sox gene cluster, mutagenesis of the flavoprotein SoxF, and evidence for a general sulfur-oxidizing system in Paracoccus pantotrophus GB17. J Bacteriol 183:4499–4508. doi: 10.1128/JB.183.15.4499-4508.2001 PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Bloem J (1995) Fluorescent staining of microbes for total direct counts. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular microbial ecology manual. Kluwer Academic Publishers, Dordrecht, pp 1–12Google Scholar
  30. 30.
    Šimek M, Virtanen S, Simojoki A, Chroňáková A, Elhottová D, Krištůfek V, Ali-Halla M (2014) The microbial communities and potential greenhouse gas production in boreal acid sulphate, non-acid sulphate, and reedy sulphidic soils. Sci Total Environ 466–467:663–672PubMedGoogle Scholar
  31. 31.
    Amann RI, 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 56:1919–1925PubMedCentralPubMedGoogle Scholar
  32. 32.
    Crocetti G, Murto M, Björnsson L (2006) An update and optimisation of oligonucleotide probes targeting methanogenic Archaea for use in fluorescence in situ hybridisation (FISH). J Microbiol Methods 65:194–201PubMedCrossRefGoogle Scholar
  33. 33.
    Daims H, Brühl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444PubMedCrossRefGoogle Scholar
  34. 34.
    Lin X, Wakeham SG, Putnam IF, Astor YM, Scranton MI, Chistoserdov AY, Taylor GT (2006) Comparison of vertical distributions of prokaryotic assemblages in the anoxic Cariaco Basin and Black Sea by use of fluorescence in situ hybridization. Appl Environ Microbiol 72:2679–2690PubMedCentralPubMedCrossRefGoogle Scholar
  35. 35.
    Loy A, Lehner A, Lee N, Adamczyk J, Meier H, Ernst J, Schleifer KH, Wagner M (2002) Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes in the environment. Appl Environ Microbiol 68:5064–5081PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Manz W, Amann R, Ludwig W, Wagner M, Schleifer K (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol 15:593–600CrossRefGoogle Scholar
  37. 37.
    Meier H, Amann R, Ludwig W, Schleifer KH (1999) Specific oligonucleotide probes for in situ detection of a major group of gram-positive bacteria with low DNA G + C content. Syst Appl Microbiol 22:186–196PubMedCrossRefGoogle Scholar
  38. 38.
    Mussmann M, Ishii K, Rabus R, Amann R (2005) Diversity and vertical distribution of cultured and uncultured Deltaproteobacteria in an intertidal mud flat of the Wadden Sea. Environ Microbiol 7:405–418PubMedCrossRefGoogle Scholar
  39. 39.
    Neef A (1997) Anwendung der in situ Einzelzell-Identifizierung von Bakterien zur Populationsanalyse in komplexen mikrobiellen Biozönosen. PhD Technische Universität München, MünchenGoogle Scholar
  40. 40.
    Sekar R, Pernthaler A, Pernthaler J, Warnecke F, Posch T, Amann R (2003) An improved protocol for quantification of freshwater Actinobacteria by fluorescence in situ hybridization. Appl Environ Microbiol 69:2928–2935PubMedCentralPubMedCrossRefGoogle Scholar
  41. 41.
    Stahl D, Amann R (1991) Development and application of nucleic acid probes. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 205–248Google Scholar
  42. 42.
    Teira E, Reinthaler T, Pernthaler A, Pernthaler J, Herndl GJ (2004) Combining catalyzed reporter deposition-fluorescence in situ hybridization and microautoradiography to detect substrate utilization by bacteria and Archaea in the deep ocean. Appl Environ Microbiol 70:4411–4414PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Wallner G, Amann R, Beisker W (1993) Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14:136–143PubMedCrossRefGoogle Scholar
  44. 44.
    Moshynets O, Koza A, Sterpaio P, Kosakivska I, Potters G, Cohen D, Spiers AJ (2011) A new plastic sampling method for the comprehensive analysis of microbial community architecture. In: Chroňáková A, Šimek M, Kyselková M, Hynšt J, Baldrian P, Pospíšek M, Krištůfek V, Elhottová D (eds) Ecology of soil microorganisms: microbes as important drivers of soil processes. Centre of Environmental Microbiology, Prague, p 384Google Scholar
  45. 45.
    Elhottová D, Krištůfek V, Tříska J, Chrastný V, Uhlířová E, Kalčík J, Picek T (2006) Immediate impact of the flood (Bohemia, August 2002) on selected soil characteristics. Water Air Soil Poll 173:177–193. doi: 10.1007/s11270-005-9054-1 CrossRefGoogle Scholar
  46. 46.
    Šimek M, Virtanen S, Krištůfek V, Simojoki A, Yli-Halla M (2011) Evidence of rich microbial communities in the subsoil of a boreal acid sulphate soil conducive to greenhouse gas emissions. Agr Ecosyst Environ 140:113–122. doi: 10.1016/j.agee.2010.11.018 CrossRefGoogle Scholar
  47. 47.
    Alden L, Demoling F, Baath E (2001) Rapid method of determining factors limiting bacterial growth in soil. Appl Environ Microb 67:1830–1838. doi: 10.1128/AEM.67.4.1830-1838.2001 CrossRefGoogle Scholar
  48. 48.
    Miseta R, Palatinszky M, Makk J, Marialigeti K, Borsodi A (2012) Phylogenetic diversity of bacterial communities associated with sulfurous karstic well waters of a Hungarian spa. Geomicrobiol J 29:101–113. doi: 10.1080/01490451.2011.558563 CrossRefGoogle Scholar
  49. 49.
    Engel A, Porter M, Stern L, Quinlan S, Bennett P (2004) Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic “Epsilonproteobacteria”. FEMS Microbiol Ecol 51:31–53. doi: 10.1016/j.femsec.2004.07.004|10.1016/j.femsec.2004.07.004 PubMedCrossRefGoogle Scholar
  50. 50.
    Pereira L, Vicentini R, Ottoboni L (2014) Changes in the bacterial community of soil from a neutral mine drainage channel. Plos One 9. doi: 10.1371/journal.pone.0096605
  51. 51.
    Serkebaeva Y, Kim Y, Liesack W, Dedysh S (2013) Pyrosequencing-based assessment of the bacteria diversity in surface and subsurface peat layers of a northern wetland, with focus on poorly studied phyla and candidate divisions. Plos One 8. doi: 10.1371/journal.pone.0063994
  52. 52.
    Campbell B, Engel A, Porter M, Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468. doi: 10.1038/nrmicro1414 PubMedCrossRefGoogle Scholar
  53. 53.
    Liu J, Hua Z, Chen L, Kuang J, Li S, Shu W, Huang L (2014) Correlating microbial diversity patterns with geochemistry in an extreme and heterogeneous environment of mine tailings. Appl Environ Microbiol 80:3677–3686. doi: 10.1128/AEM.00294-14 PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.
    Wright KE, Williamson C, Grasby SE, Spear JR, Templeton AS (2013) Metagenomic evidence for sulfur lithotrophy by Epsilonproteobacteria as the major energy source for primary productivity in a sub-aerial arctic glacial deposit, Borup Fiord Pass. Front Microbiol 4(63):1–20. doi: 10.3389/fmicb.2013.00063
  55. 55.
    Shao M, Zhang T, Fang H (2010) Sulfur-driven autotrophic denitrification: diversity, biochemistry, and engineering applications. Appl Microbiol Biot 88:1027–1042. doi: 10.1007/s00253-010-2847-1 CrossRefGoogle Scholar
  56. 56.
    Hayakawa A, Hatakeyama M, Asano R, Ishikawa Y, Hidaka S (2013) Nitrate reduction coupled with pyrite oxidation in the surface sediments of a sulfide-rich ecosystem. J Geophys Res-Biogeo 118:639–649. doi: 10.1002/jgrg.20060 CrossRefGoogle Scholar
  57. 57.
    Beller H, Letain T, Chakicherla A, Kane S, Legler T, Coleman M (2006) Whole-genome transcriptional analysis of chemolithoautotrophic thiosulfate oxidation by Thiobacillus denitrificans under aerobic versus denitrifying conditions. J Bacteriol 188:7005–7015. doi: 10.1128/JB.00568-06 PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Schedel M, Truper H (1980) Anaerobic oxidation of thiosulfate and elemental sulfur in Thiobacillus denitrificans. Arch Microbiol 124:205–210. doi: 10.1007/BF00427728 CrossRefGoogle Scholar
  59. 59.
    Zhang M, Zhang T, Shao M, Fang H (2009) Autotrophic denitrification in nitrate-induced marine sediment remediation and Sulfurimonas denitrificans-like bacteria. Chemosphere 76:677–682. doi: 10.1016/j.chemosphere.2009.03.066 PubMedCrossRefGoogle Scholar
  60. 60.
    Chen Y, Wu L, Boden R, Hillebrand A, Kumaresan D, Moussard H, Baciu M, Lu Y, Murrell J (2009) Life without light: microbial diversity and evidence of sulfur- and ammonium-based chemolithotrophy in Movile Cave. ISME J 3:1093–1104. doi: 10.1038/ismej.2009.57 PubMedCrossRefGoogle Scholar
  61. 61.
    Kodama Y, Watanabe K (2004) Sulfuricurvum kujiense gen. nov., sp nov., a facultatively anaerobic, chemolithoautotrophic, sulfur-oxidizing bacterium isolated from an underground crude-oil storage cavity. Int J Syst Evol Micr 54:2297–2300. doi: 10.1099/ijs.0.63243-0 CrossRefGoogle Scholar
  62. 62.
    Sarbu S, Kane T, Kinkle B (1996) A chemoautotrophically based cave ecosystem. Science 272:1953–1955. doi: 10.1126/science.272.5270.1953 PubMedCrossRefGoogle Scholar
  63. 63.
    Darcy J, Lynch R, King A, Robeson M, Schmidt S (2011) Global distribution of Polaromonas phylotypes - evidence for a highly successful dispersal capacity. Plos One 6. doi: 10.1371/journal.pone.0023742
  64. 64.
    Loy A, Beisker W, Meier H (2005) Diversity of bacteria growing in natural mineral water after bottling. Appl Environ Microb 71:3624–3632. doi: 10.1128/AEM.71.7.3624-3632.2005 CrossRefGoogle Scholar
  65. 65.
    Sizova M, Panikov N (2007) Appl Environ Microb sp. nov., a psychrotolerant hydrogen-oxidizing bacterium from Alaskan soil. Int J Syst Evol Micr 57:616–619. doi: 10.1099/ijs.0.64350-0 CrossRefGoogle Scholar
  66. 66.
    Giloteaux L, Sole A, Esteve I, Duran R (2011) Bacterial community composition characterization of a lead-contaminated Microcoleus sp consortium. Environ Sci Pollut R 18:1147–1159. doi: 10.1007/s11356-010-0432-x CrossRefGoogle Scholar
  67. 67.
    Yair S, Yaacov D, Susan K, Jurkevitch E (2003) Small eats big: ecology and diversity of Bdellovibrio and like organisms, and their dynamics in predator–prey interactions. Agronomie 23:433–439. doi: 10.1051/agro:2003026 CrossRefGoogle Scholar
  68. 68.
    Rendulic S, Jagtap P, Rosinus A, Eppinger M, Baar C, Lanz C, Keller H, Lambert C, Evans K, Goesmann A, Meyer F, Sockett R, Schuster S (2004) A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 303:689–692. doi: 10.1126/science.1093027 PubMedCrossRefGoogle Scholar
  69. 69.
    Hedman P, Ringertz O, Lindström M, Olsson K (1993) The origin of Staphylococcus saprophyticus from cattle and pigs. Scand J Infect Dis 25:57–60PubMedCrossRefGoogle Scholar
  70. 70.
    Verhille S, Baida N, Dabboussi F, Izard D, Leclerc H (1999) Taxonomic study of bacteria isolated from natural mineral waters: proposal of Pseudomonas jessenii sp. nov. and Pseudomonas mandelii sp. nov. Syst Appl Microbiol 22:45–58PubMedCrossRefGoogle Scholar
  71. 71.
    Lim Y, Shin K, Kim J (2007) Distinct antimicrobial resistance patterns and antimicrobial resistance-harboring genes according to genomic species of Acinetobacter isolates. J Clin Microbiol 45:902–905. doi: 10.1128/JCM.01573-06 PubMedCentralPubMedCrossRefGoogle Scholar
  72. 72.
    Straganz G, Glieder A, Brecker L, Ribbons D, Steiner W (2003) Acetylacetone-cleaving enzyme Dke1: a novel C–C-bond-cleaving enzyme from Acinetobacter johnsonii. Biochem J 369:573–581. doi: 10.1042/BJ20021047 PubMedCentralPubMedCrossRefGoogle Scholar
  73. 73.
    Boswell C, Dick R, Eccles H, Macaskie L (2001) Phosphate uptake and release by Acinetobacter johnsonii in continuous culture and coupling of phosphate release to heavy metal accumulation. J Ind Microbiol Biot 26:333–340. doi: 10.1038/sj.jim.7000139 CrossRefGoogle Scholar
  74. 74.
    Jiang Y, Zhang X, Chen G, Shen Y, Zhou L (2012) The pilot study for waste oil removal from oilfields by Acinetobacter johnsonii using a specialized batch bioreactor. Biotechnol Bioproc E 17:1300–1305. doi: 10.1007/s12257-012-0232-x CrossRefGoogle Scholar
  75. 75.
    Yoon B, Lee D, Kang Y, Oh D, Kim S, Oh K, Kahng H (2002) Evaluation of carbazole degradation by Pseudomonas rhodesiae strain KK1 isolated from soil contaminated with coal tar. J Basic Microb 42:434–443. doi: 10.1002/1521-4028(200212)42:6<434::AID-JOBM434>3.0.CO;2-C CrossRefGoogle Scholar
  76. 76.
    Fontanille P, Le Fleche A, Larroche C (2002) Pseudomonas rhodesiae PF1: a new and efficient biocatalyst for production of isonovalal from alpha-pinene oxide. Biocatal Biotransfor 20:413–421. doi: 10.1080/1024242021000058702 CrossRefGoogle Scholar
  77. 77.
    Kahng H, Nam K, Kukor J, Yoon B, Lee D, Oh D, Kam S, Oh K (2002) PAH utilization by Pseudomonas rhodesiae KK1 isolated from a former manufactured-gas plant site. Appl Microbiol Biot 60:475–480. doi: 10.1007/s00253-002-1137-y CrossRefGoogle Scholar
  78. 78.
    Anbu P (2014) Characterization of an extracellular lipase by Pseudomonas koreensis BK-L07 isolated from soil. Prep Biochem Biotech 44:266–280. doi: 10.1080/10826068.2013.812564 CrossRefGoogle Scholar
  79. 79.
    Friedrich C, Bardischewsky F, Rother D, Quentmeier A, Fischer J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8:253–259. doi: 10.1016/j.mib.2005.04.005 PubMedCrossRefGoogle Scholar
  80. 80.
    Claus G, Kutzner H (1985) Physiology and kinetics of autotrophic denitrification by Thiobacillus denitrificans. Appl Microbiol Biot 22:283–288Google Scholar
  81. 81.
    Che X, Luo GZ, Tan HX, Wu JM, Jiang Y, Qi JL, Sun DC (2008) Isolation, identification and denitrification characterization of Thiobacillus denitrificans. Huan jing ke xue 29:2931–2937PubMedGoogle Scholar
  82. 82.
    Warscheid T, Braams J (2000) Biodeterioration of stone: a review. Int Biodeter Biodeg 46:343–368. doi: 10.1016/S0964-8305(00)00109-8 CrossRefGoogle Scholar
  83. 83.
    Krajewska B, van Eldik R, Brindell M (2012) Temperature- and pressure-dependent stopped-flow kinetic studies of jack bean urease. Implications for the catalytic mechanism. J Biol Inorg Chem 17:1123–1134. doi: 10.1007/s00775-012-0926-8 PubMedCentralPubMedCrossRefGoogle Scholar
  84. 84.
    Mahmood Q, Zheng P, Cai J, Hayat Y, Hassan M, Wu D, Hu B (2007) Sources of sulfide in waste streams and current biotechnologies for its removal. J Zhejiang Univ-Sc A 8:1126–1140. doi: 10.1631/jzus.2007.A1126 CrossRefGoogle Scholar
  85. 85.
    Chuan MC, Shu GY, Liu JC (1996) Solubility of heavy metals in a contaminated soil: effects of redox potential and pH. Water Air Soil Poll 90:543–556. doi: 10.1007/BF00282668 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Janez Mulec
    • 1
  • Václav Krištůfek
    • 2
  • Alica Chroňáková
    • 2
  • Andreea Oarga
    • 3
  • Josef Scharfen
    • 4
    • 5
  • Martina Šestauberová
    • 2
  1. 1.Research Centre of the Slovenian Academy of Sciences and ArtsKarst Research InstitutePostojnaSlovenia
  2. 2.Biology Centre of the Academy of Sciences of the Czech Republicv. v. i.-Institute of Soil BiologyČeské BudějoviceCzech Republic
  3. 3.Ştefan cel Mare UniversitySuceavaRomania
  4. 4.Department of Clinical Microbiology, Faculty of Medicine and University HospitalCharles UniversityHradec KralovéCzech Republic
  5. 5.National Reference Laboratory for Pathogenic Actinomycetes, Department of Medical Microbiology and ImmunologyRegional Hospital Trutnov, Inc.TrutnovCzech Republic

Personalised recommendations