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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000205
2016-01-01
2020-02-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/1/62.html?itemId=/content/journal/micro/10.1099/mic.0.000205&mimeType=html&fmt=ahah

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 Ecol45:317–328 [CrossRef][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 Microbiol32:140–150 [CrossRef][PubMed]
    [Google Scholar]
  3. Baker-Austin C., Dopson M.. 2007; Life in acid: pH homeostasis in acidophiles. Trends Microbiol15:165–171 [CrossRef][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 Microbiol66:3842–3849 [CrossRef][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 Microbiol64:2181–2186[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 Microbiol77:545–554 [CrossRef][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 Spectrosc68:212–219 [CrossRef]
    [Google Scholar]
  8. Clark D. A., Norris P. R.. 1996; Acidimicrobium ferrooxidans gen. nov. sp. nov.: mixed-culture ferrous iron oxidation with Sulfobacillus species. Microbiology142:785–790[CrossRef]
    [Google Scholar]
  9. Colmer A. R., Hinkle M. E.. 1947; The role of microorganisms in acid mine drainage: a preliminary report. Science106:253–256 [CrossRef][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 Trans5:13–32 [CrossRef]
    [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 J16:155–179 [CrossRef]
    [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 Announc3:e00382–e00315 [CrossRef][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 Ecol87:231–243 [CrossRef][PubMed]
    [Google Scholar]
  14. Frankel R. B., Bazylinski D. A.. 2003; Biologically induced mineralization by bacteria. Rev Mineral Geochem54:95–114 [CrossRef]
    [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 Environ27:19–29 [CrossRef][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 Ecol81:303–314 [CrossRef][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 pp3–14 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 Microbiol77:2685–2694 [CrossRef][PubMed]
    [Google Scholar]
  19. Grossart H. P., Ploug H.. 2000; Bacterial production and growth efficiencies: direct measurements on riverine aggregates. Limnol Oceanogr45:436–445 [CrossRef]
    [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 Microbiol72:2022–2030 [CrossRef][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 Technol45:7685–7692 [CrossRef][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 Microbiol61:1281–1285[PubMed][CrossRef]
    [Google Scholar]
  23. Johnson D. B., Hallberg K. B.. 2007; Techniques for detecting and identifying acidophilic mineral-oxidizing microorganisms. In Biomining pp237–261 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 Microbiol180:60–68 [CrossRef][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 Res36:W5–W9 [CrossRef][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 Microbiol59:1082–1089 [CrossRef][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 Microbiol166:111–120 [CrossRef][PubMed]
    [Google Scholar]
  28. Kappler A., Straub K. L.. 2005; Geomicrobiological cycling of iron. Rev Mineral Geochem59:85–108 [CrossRef]
    [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 Hydrobiol80:639–653 [CrossRef]
    [Google Scholar]
  31. Küsel K.. 2003; Microbial cycling of iron and sulfur in acidic coal mining lake sediments. Water Air Soil Pollut Focus3:67–90 [CrossRef]
    [Google Scholar]
  32. Lane D. J.. 1991; 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics pp115–175 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 Rev14:103–119 [CrossRef]
    [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 Ecol41:20–35[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 Lett235:221–228 [CrossRef][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 Microbiol76:8174–8183 [CrossRef][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 Microbiol79:4272–4281 [CrossRef][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 Res32:1363–1371 [CrossRef][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 Biol52:1043–1057 [CrossRef]
    [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 J8:1259–1274 [CrossRef][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 Microbiol68:3988–3995 [CrossRef][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 Biochem40:312–321 [CrossRef]
    [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 pp115–142 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 Geol283:134–142 [CrossRef]
    [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 Ser179:1–11 [CrossRef]
    [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 Oceanogr56:1386–1398 [CrossRef]
    [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 Microbiol9:1761–1771 [CrossRef][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 One8:e66746 [CrossRef][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). Talanta21:314–318 [CrossRef][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 Methods95:138–144 [CrossRef][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. Nature428:37–43 [CrossRef][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 Ecol64:91–104 [CrossRef][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 Microbiol31:17–28 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000205
Loading
/content/journal/micro/10.1099/mic.0.000205
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error