1887

Abstract

A new acidophilic iron-oxidizing strain (C25) belonging to the novel genus was isolated from pelagic iron-rich aggregates (‘iron snow’) collected below the redoxcline of an acidic lignite mine lake. Strain C25 catalysed the oxidation of ferrous iron [Fe(II)] under oxic conditions at 25 °C at a rate of 3.8 mM Fe(II) day in synthetic medium and 3.0 mM Fe(II) day in sterilized lake water in the presence of yeast extract, producing the rust-coloured, poorly crystalline mineral schwertmannite [Fe(III) oxyhydroxylsulfate]. During growth, rod-shaped cells of strain C25 formed long filaments, and then aggregated and degraded into shorter fragments, building large cell–mineral aggregates in the late stationary phase. Scanning electron microscopy analysis of cells during the early growth phase revealed that Fe(III)-minerals were formed as single needles on the cell surface, whereas the typical pincushion-like schwertmannite was observed during later growth phases at junctions between the cells, leaving major parts of the cell not encrusted. This directed mechanism of biomineralization at specific locations on the cell surface has not been reported from other acidophilic iron-oxidizing bacteria. Strain C25 was also capable of reducing Fe(III) under micro-oxic conditions which led to a dissolution of the Fe(III)-minerals. Thus, strain C25 appeared to have ecological relevance for both the formation and transformation of the pelagic iron-rich aggregates at oxic/anoxic transition zones in the acidic lignite mine lake.

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2016-01-01
2024-03-29
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References

  1. Alfreider A., Vogt C., Hoffmann D., Babel W. 2003; Diversity of ribulose-1,5-bisphosphate carboxylase/oxygenase large-subunit genes from groundwater and aquifer microorganisms. Microb Ecol 45:317–328 [View Article][PubMed]
    [Google Scholar]
  2. Alfreider A., Vogt C., Geiger-Kaiser M., Psenner R. 2009; Distribution and diversity of autotrophic bacteria in groundwater systems based on the analysis of RubisCO genotypes. Syst Appl Microbiol 32:140–150 [View Article][PubMed]
    [Google Scholar]
  3. Baker-Austin C., Dopson M. 2007; Life in acid: pH homeostasis in acidophiles. Trends Microbiol 15:165–171 [View Article][PubMed]
    [Google Scholar]
  4. Bond P. L., Smriga S. P., Banfield J. F. 2000; Phylogeny of microorganisms populating a thick, subaerial, predominantly lithotrophic biofilm at an extreme acid mine drainage site. Appl Environ Microbiol 66:3842–3849 [View Article][PubMed]
    [Google Scholar]
  5. Bridge T.A.M., Johnson D. B. 1998; Reduction of soluble iron and reductive dissolution of ferric iron-containing minerals by moderately thermophilic iron-oxidizing bacteria. Appl Environ Microbiol 64:2181–2186[PubMed]
    [Google Scholar]
  6. Brown J. F., Jones D. S., Mills D. B., Macalady J. L., Burgos W. D. 2011; Application of a depositional facies model to an acid mine drainage site. Appl Environ Microbiol 77:545–554 [View Article][PubMed]
    [Google Scholar]
  7. Ciobotă V., Lu S., Tarcea N., Rösch P., Küsel K., Popp J. 2013; Quantification of the inorganic phase of the pelagic aggregates from an iron contaminated lake by means of Raman spectroscopy. Vib Spectrosc 68:212–219 [View Article]
    [Google Scholar]
  8. Clark D. A., Norris P. R. 1996; Acidimicrobium ferrooxidans gen. nov. sp. nov.: mixed-culture ferrous iron oxidation with Sulfobacillus species. Microbiology 142:785–790 [CrossRef]
    [Google Scholar]
  9. Colmer A. R., Hinkle M. E. 1947; The role of microorganisms in acid mine drainage: a preliminary report. Science 106:253–256 [View Article][PubMed]
    [Google Scholar]
  10. Druschel G. K., Baker B. J., Gihring T. M., Banfield J. F. 2004; Acid mine drainage biogeochemistry at Iron Mountain, California. Geochem Trans 5:13–32 [View Article]
    [Google Scholar]
  11. Edwards K. J., Goebel B. M., Rodgers T. M., Schrenk M. O., Gihring T. M., Cardona M. M., Hu B., McGuire M. M., Hamers R. J., Pace N. R., Banfield J. F. 1999; Geomicrobiology of pyrite (FeS2) dissolution: case study at Iron Mountain, California. Geomicrobiol J 16:155–179 [View Article]
    [Google Scholar]
  12. Eisen S., Poehlein A., Johnson D. B., Daniel R., Schlömann M., Mühling M. 2015; Genome sequence of the acidophilic ferrous iron-oxidizing isolate Acidithrix ferrooxidans strain Py-F3, the proposed type strain of the novel actinobacterial genus Acidithrix . Genome Announc 3:e00382–e00315 [View Article][PubMed]
    [Google Scholar]
  13. Falagán C., Sánchez-España J., Johnson D. B. 2014; New insights into the biogeochemistry of extremely acidic environments revealed by a combined cultivation-based and culture-independent study of two stratified pit lakes. FEMS Microbiol Ecol 87:231–243 [View Article][PubMed]
    [Google Scholar]
  14. Frankel R. B., Bazylinski D. A. 2003; Biologically induced mineralization by bacteria. Rev Mineral Geochem 54:95–114 [View Article]
    [Google Scholar]
  15. Fujimura R., Sato Y., Nishizawa T., Nanba K., Oshima K., Hattori M., Kamijo T., Ohta H. 2012; Analysis of early bacterial communities on volcanic deposits on the island of Miyake (Miyake-jima), Japan: a 6-year study at a fixed site. Microbes Environ 27:19–29 [View Article][PubMed]
    [Google Scholar]
  16. García-Moyano A., González-Toril E., Aguilera Á., Amils R. 2012; Comparative microbial ecology study of the sediments and the water column of the Río Tinto, an extreme acidic environment. FEMS Microbiol Ecol 81:303–314 [View Article][PubMed]
    [Google Scholar]
  17. Geller W., Klapper H., Schultze M. 1998; Natural and anthropogenic sulforic acidification of lakes. In Acid Mining Lakes: Acid Mine Drainage, Limnology and Reclamation pp 3–14 Edited by Geller W., Klapper H., Salomons W. Berlin: Springer;
    [Google Scholar]
  18. González-Toril E., Aguilera A., Souza-Egipsy V., López Pamo E., Sánchez España J., Amils R. 2011; Geomicrobiology of La Zarza-Perrunal acid mine effluent (Iberian Pyritic Belt, Spain). Appl Environ Microbiol 77:2685–2694 [View Article][PubMed]
    [Google Scholar]
  19. Grossart H. P., Ploug H. 2000; Bacterial production and growth efficiencies: direct measurements on riverine aggregates. Limnol Oceanogr 45:436–445 [View Article]
    [Google Scholar]
  20. Hallberg K. B., Coupland K., Kimura S., Johnson D. B. 2006; Macroscopic streamer growths in acidic, metal-rich mine waters in north Wales consist of novel and remarkably simple bacterial communities. Appl Environ Microbiol 72:2022–2030 [View Article][PubMed]
    [Google Scholar]
  21. Hedrich S., Lünsdorf H., Kleeberg R., Heide G., Seifert J., Schlömann M. 2011; Schwertmannite formation adjacent to bacterial cells in a mine water treatment plant and in pure cultures of Ferrovum myxofaciens . Environ Sci Technol 45:7685–7692 [View Article][PubMed]
    [Google Scholar]
  22. Itoh T., Yamanoi K., Kudo T., Ohkuma M., Takashina T. 2011; Aciditerrimonas ferrireducens gen. nov., sp. nov., an iron-reducing thermoacidophilic actinobacterium isolated from a solfataric field. Int J Syst Evol Microbiol 61:1281–1285[PubMed] [CrossRef]
    [Google Scholar]
  23. Johnson D. B., Hallberg K. B. 2007; Techniques for detecting and identifying acidophilic mineral-oxidizing microorganisms. In Biomining pp 237–261 Edited by Rawlings D. E., Johnson D. B. Berlin: Springer; [CrossRef]
    [Google Scholar]
  24. Johnson D. B., Okibe N., Roberto F. F. 2003; Novel thermo-acidophilic bacteria isolated from geothermal sites in Yellowstone National Park: physiological and phylogenetic characteristics. Arch Microbiol 180:60–68 [View Article][PubMed]
    [Google Scholar]
  25. Johnson M., Zaretskaya I., Raytselis Y., Merezhuk Y., McGinnis S., Madden T. L. 2008; NCBI blast: a better web interface. Nucleic Acids Res 36:W5–W9 [View Article][PubMed]
    [Google Scholar]
  26. Johnson D. B., Bacelar-Nicolau P., Okibe N., Thomas A., Hallberg K. B. 2009; Ferrimicrobium acidiphilum gen. nov. sp. nov. and Ferrithrix thermotolerans gen. nov., sp. nov.: heterotrophic, iron-oxidizing, extremely acidophilic actinobacteria. Int J Syst Evol Microbiol 59:1082–1089 [View Article][PubMed]
    [Google Scholar]
  27. Jones R. M., Johnson D. B. 2015; Acidithrix ferrooxidans gen. nov. sp. nov., a filamentous and obligately heterotrophic, acidophilic member of the Actinobacteria that catalyzes dissimilatory oxido-reduction of iron. Res Microbiol 166:111–120 [View Article][PubMed]
    [Google Scholar]
  28. Kappler A., Straub K. L. 2005; Geomicrobiological cycling of iron. Rev Mineral Geochem 59:85–108 [View Article]
    [Google Scholar]
  29. Kay C. M., Rowe O. F., Rocchetti L., Coupland K., Hallberg K. B., Johnson D. B. 2013; Evolution of microbial “streamer” growths in an acidic, metal-contaminated stream draining an abandoned underground copper mine. In Life 3, 189–210
    [Google Scholar]
  30. Klapper H., Schultze M. 1995; Geogenically acidified mining lakes - living conditions and possibilities of restoration. Int Rev Hydrobiol 80:639–653 [View Article]
    [Google Scholar]
  31. Küsel K. 2003; Microbial cycling of iron and sulfur in acidic coal mining lake sediments. Water Air Soil Pollut Focus 3:67–90 [View Article]
    [Google Scholar]
  32. Lane D. J. 1991; 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics pp 115–175 Edited by Stackebrandt E., Goodfellow M. New York: Wiley;
    [Google Scholar]
  33. Leduc L. G., Ferroni G. D. 1994; The chemolithotrophic bacterium Thiobacillus ferrooxidans . FEMS Microbiol Rev 14:103–119 [View Article]
    [Google Scholar]
  34. López-Archilla A. I., Marin I., Amils R. 2001; Microbial community composition and ecology of an acidic aquatic environment: the Tinto River, Spain. Microb Ecol 41:20–35[PubMed]
    [Google Scholar]
  35. López-Archilla A. I., Gérard E., Moreira D., López-García P. 2004; Macrofilamentous microbial communities in the metal-rich and acidic River Tinto, Spain. FEMS Microbiol Lett 235:221–228 [View Article][PubMed]
    [Google Scholar]
  36. Lu S., Gischkat S., Reiche M., Akob D. M., Hallberg K. B., Küsel K. 2010; Ecophysiology of Fe-cycling bacteria in acidic sediments. Appl Environ Microbiol 76:8174–8183 [View Article][PubMed]
    [Google Scholar]
  37. Lu S., Chourey K., Reiche M., Nietzsche S., Shah M. B., Neu T. R., Hettich R. L., Küsel K. 2013; Insights into the structure and metabolic function of microbes that shape pelagic iron-rich aggregates (iron snow). Appl Environ Microbiol 79:4272–4281 [View Article][PubMed]
    [Google Scholar]
  38. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Yadhukumar, Buchner A., Lai T., Steppi S., other authors. 2004; arb: a software environment for sequence data. Nucleic Acids Res 32:1363–1371 [View Article][PubMed]
    [Google Scholar]
  39. Luef B., Aspetsberger F., Hein T., Huber F., Peduzzi P. 2007; Impact of hydrology on free-living and particle-associated microorganisms in a river floodplain system (Danube, Austria). Freshw Biol 52:1043–1057 [View Article]
    [Google Scholar]
  40. Méndez-García C., Mesa V., Sprenger R. R., Richter M., Diez M. S., Solano J., Bargiela R., Golyshina O. V., Manteca Á., other authors. 2014; Microbial stratification in low pH oxic and suboxic macroscopic growths along an acid mine drainage. ISME J 8:1259–1274 [View Article][PubMed]
    [Google Scholar]
  41. Neubauer S. C., Emerson D., Megonigal J. P. 2002; Life at the energetic edge: kinetics of circumneutral iron oxidation by lithotrophic iron-oxidizing bacteria isolated from the wetland-plant rhizosphere. Appl Environ Microbiol 68:3988–3995 [View Article][PubMed]
    [Google Scholar]
  42. Nicomrat D., Dick W. A., Dopson M., Tuovinen O. H. 2008; Bacterial phylogenetic diversity in a constructed wetland system treating acid coal mine drainage. Soil Biol Biochem 40:312–321 [View Article]
    [Google Scholar]
  43. Nixdorf B., Hemm M., Schlundt A., Kapfer M., Krumbeck H. 2001 Tagebauseen in Deutschland – ein Überblick [Mining Lakes in Germany – An Overview] Berlin: UBA Texte;
    [Google Scholar]
  44. Norris P., Ingledew W., Herbert R., Sharp R. 1992; Acidophilic bacteria: adaptations and applications. In Molecular Biology and Biotechnology of Extremophiles pp 115–142 Edited by Herbert R. A., Sharp R. J. Glasgow: Blackie; [CrossRef]
    [Google Scholar]
  45. Paikaray S., Göttlicher J., Peiffer S. 2011; Removal of As(III) from acidic waters using schwertmannite: surface speciation and effect of synthesis pathway. Chem Geol 283:134–142 [View Article]
    [Google Scholar]
  46. Ploug H., Grossart H. P., Azam F., Jorgensen B. B. 1999; Photosynthesis, respiration, and carbon turnover in sinking marine snow from surface waters of Southern California Bight: implications for the carbon cycle in the ocean. Mar Ecol Prog Ser 179:1–11 [View Article]
    [Google Scholar]
  47. Reiche M., Lu S., Ciobota V., Neu T. R., Nietzsche S., Rösch P., Popp J., Küsel K. 2011; Pelagic boundary conditions affect the biological formation of iron-rich particles (iron snow) and their microbial communities. Limnol Oceanogr 56:1386–1398 [View Article]
    [Google Scholar]
  48. Rowe O. F., Sánchez-España J., Hallberg K. B., Johnson D. B. 2007; Microbial communities and geochemical dynamics in an extremely acidic, metal-rich stream at an abandoned sulfide mine (Huelva, Spain) underpinned by two functional primary production systems. Environ Microbiol 9:1761–1771 [View Article][PubMed]
    [Google Scholar]
  49. Santofimia E., González-Toril E., López-Pamo E., Gomariz M., Amils R., Aguilera A. 2013; Microbial diversity and its relationship to physicochemical characteristics of the water in two extreme acidic pit lakes from the Iberian pyrite belt (SW Spain). PLoS One 8:e66746 [View Article][PubMed]
    [Google Scholar]
  50. Tamura H., Goto K., Yotsuyanagi T., Nagayama M. 1974; Spectrophotometric determination of iron(II) with 1,10-phenanthroline in the presence of large amounts of iron(III). Talanta 21:314–318 [View Article][PubMed]
    [Google Scholar]
  51. Tischler J. S., Jwair R. J., Gelhaar N., Drechsel A., Skirl A.-M., Wiacek C., Janneck E., Schlömann M. 2013; New cultivation medium for Ferrovum and Gallionella-related strains. J Microbiol Methods 95:138–144 [View Article][PubMed]
    [Google Scholar]
  52. Tyson G. W., Chapman J., Hugenholtz P., Allen E. E., Ram R. J., Richardson P. M., Solovyev V. V., Rubin E. M., Rokhsar D. S., Banfield J. F. 2004; Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43 [View Article][PubMed]
    [Google Scholar]
  53. Urbieta M. S., González Toril E., Aguilera A., Giaveno M. A., Donati E. 2012; First prokaryotic biodiversity assessment using molecular techniques of an acidic river in Neuquén, Argentina. Microb Ecol 64:91–104 [View Article][PubMed]
    [Google Scholar]
  54. Wakao N., Tachibana H., Tanaka Y., Sakurai Y., Shiota H. 1985; Morphological and physiological characteristics of streamers in acid mine drainage water from a pyritic mine. J Gen Appl Microbiol 31:17–28 [View Article]
    [Google Scholar]
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