Oxygen-dependent niche formation of a pyrite-dependent acidophilic consortium built by archaea and bacteria

ISME Journal

Volumn 7, Issue 9, 2013, Pages 1725-1737

  Ziegler, Sibylle ^a,b   Dolch, Kerstin ^b   Geiger, Katharina ^b   Krause, Susanne ^b   Asskamp, Maximilian ^a   Eusterhues, Karin ^c   Kriews, Michael ^d   Wilhelms Dick, Dorothee ^e   Goettlicher, Joerg ^b   Majzlan, Juraj ^c   Gescher, Johannes ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^d ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^e UNIVERSITY OF BREMEN   (Germany)

Author keywords

acid mine drainage; Acidithionbacillus; ARMAN; ecological niche; Leptospririllum; thermoplasmatales

Indexed keywords

IRON; OXYGEN; PYRITE; RNA 16S; SULFIDE;

ACID MINE DRAINAGE; ANOXIC CONDITIONS; BACTERIUM; BIOFILM; FIXATION; FLUORESCENCE; HYBRIDIZATION; MICROBIAL ACTIVITY; OXYGEN; PH; PRIMARY PRODUCTION; X-RAY;

AEROBIC METABOLISM; ANAEROBIC GROWTH; ARCHAEON; ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; BIODIVERSITY; BIOFILM; CARBON CYCLE; GENETICS; METABOLISM; MICROBIAL CONSORTIUM; MINING; PH; PHYLOGENY; PHYSIOLOGY;

AEROBIOSIS; ANAEROBIOSIS; ARCHAEA; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIODIVERSITY; BIOFILMS; CARBON CYCLE; HYDROGEN-ION CONCENTRATION; IRON; MICROBIAL CONSORTIA; MINING; OXYGEN; PHYLOGENY; RNA, RIBOSOMAL, 16S; SULFIDES;

ARCHAEA; BACTERIA (MICROORGANISMS); LEPTOSPIRILLUM FERROOXIDANS; THERMOPLASMATALES;

EID: 84883150669     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.64     Document Type: Article

References (43)

1. Amaral-Zettler LA, Zettler ER, Theroux SM, Palacios C, Aguilera A, Amils R. (2011). Microbial community structure across the tree of life in the extreme Rio Tinto. ISME J 5: 42-50
2. Baker BJ, Comolli LR, Dick GJ, Hauser LJ, Hyatt D, Dill BD et al. (2010). Enigmatic, ultrasmall, uncultivated Archaea. Proc Natl Acad Sci USA 107: 8806-8811
3. Baker BJ, Tyson GW, Webb RI, Flanagan J, Hugenholtz P, Allen EE et al. (2006). Lineages of acidophilic archaea revealed by community genomic analysis. Science 314: 1933-1935
4. Balashova VV, Vedenina IY, Markosyan GE, Zavarzin GA. (1973). The auxotrophic growth of Leptospirillum ferrooxidans. Mikrobiologiya 43: 581-585
5. Bond PL, Druschel GK, Banfield JF. (2000). Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems. Appl Environ Microbiol 66: 4962-4971
6. Brioukhanov AL, Netrusov AI. (2004). Catalase and superoxide dismutase: Distribution, properties, and physiological role in cells of strict anaerobes. Biochemistry 69: 949-962
7. Brown JF, Jones DS, Mills DB, Macalady JL, Burgos WD. (2011). Application of a depositional facies model to an acid mine drainage site. Appl Environ Microbiol 77: 545-554
8. Clark WM. (1960). Oxidation-Reduction Potentials of Organic Systems. Waverly Press: Baltimore, MD, USA
9. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ et al. (2009). The Ribosomal Database Project: Improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145
10. Dopson M, Baker-Austin C, Hind A, Bowman JP, Bond PL. (2004). Characterization of Ferroplasma isolates and Ferroplasma acidarmanus sp. nov., extreme acidophiles from acid mine drainage and industrial bioleaching environments. Appl Environ Microb 70: 2079-2088
11. Elias DA, Krumholz LR, Tanner RS, Sulfita JM. (1999). Estimation of methanogen biomass by quantitation of coenzyme M. Appl Environ Micobiol 65: 5541-5545
12. Gale NL, Beck JV. (1967). Evidence for the calvin cycle and hexose monophosphate pathway in Thiobacillus ferrooxidans. J Bacteriol 94: 1052-1059
13. García-Moyano A, González-Toril E, Aguilera A, Amils R. (2007). Prokaryotic community composition and ecology of floating macroscopic filaments from an extreme acidic environment, Río Tinto (SW, Spain). Syst Appl Microbiol 30: 601-614
14. Golyshina OV, Pivovarova TA, Karavaiko GI, Kondrateva TF, Moore ER, Abraham WR et al. (2000). Ferroplasma acidiphilum gen. nov., sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing, cell-wall-lacking, mesophilic member of the Ferroplasmaceae fam. nov., comprising a distinct lineage of the Archaea. Int J Syst Evol Microbiol 50(Pt 3): 997-1006
15. Gonzalez-Toril E, Aguilera A, Souza-Egipsy V, Lopez Pamo E, Sanchez Espana J, Amils R. (2011). Geomicrobiology of La Zarza-Perrunal acid mine effluent (Iberian Pyritic Belt, Spain). Appl Environ Microbiol 77: 2685-2694
16. Hallberg KB. (2010). New perspectives in acid mine drainage microbiology. Hydrometallurgy 104: 448-453
17. Hallberg KB, Coupland K, Kimura S, Johnson DB. (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
18. Hippe H. (2000). Leptospirillum gen. nov. (ex Markosyan 1972), nom. rev., including Leptospirillum ferrooxidans sp. nov. (ex Markosyan 1972), nom. rev. and Leptospirillum thermoferrooxidans sp. nov. (Golovacheva et al. 1992). Int J Syst Evol Microbiol 50(Pt 2): 501-503
19. Huber R, Stetter KO. (2001). Thermoplasmatales. In: The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) Springer: New York, NY, USA
20. Johnson DB, Hallberg KB. (2005). Acid mine drainage remediation options: A review. Sci Total Environ 338: 3-14
21. Johnson DB, McGinness S. (1991). Ferric iron reduction by acidophilic heterotrophic bacteria. Appl Environ Microbiol 57: 207-211
22. Jones D, Brown J, Larson L, Mills D, Burgos W, Macalady J. (2011). Ecological niches of Fe-oxidizing acidophiles in a coal mine discharge. In Goldschmidt Abstracts 2011. Mineral Mag 75: 1092-1131
23. Kimura S, Bryan CG, Hallberg KB, Johnson DB. (2011). Biodiversity and geochemistry of an extremely acidic, low-temperature subterranean environment sustained by chemolithotrophy. Environ Microbiol 13: 2092-2104
24. Kolmert A, Wikstrom P, Hallberg KB. (2000). A fast and simple turbidimetric method for the determination of sulfate in sulfate-reducing bacterial cultures. J Microbiol Methods 41: 179-184
25. Kriews M, Dunker E, Reinhardt H, Beninga I, Hoffmann E, Lüdtke C. (2001). Patentschrift DE000019934561C2
26. Kriews M, Reinhardt H, Dunker E, Beninga I, Ruhe W. (2004). Utility Patent DE 20 2004 005 9916
27. Lo I, Denef VJ, VerBerkmoes NC, Shah MB, Goltsman D, DiBartolo G et al. (2007). Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446: 537-541
28. Maciag WJ, Lundgren DG. (1964). Carbon dioxide fixation in the chemoautotroph, Ferrobacillus ferrooxidans. Biochem Biophys Res Commun 17: 603-607
29. Maklashina E, Berthold DA, Cecchini G. (1998). Anaerobic expression of Escherichia coli succinate dehydrogenase: Functional replacement of fumarate reductase in the respiratory chain during anaerobic growth. J Bacteriol 180: 5989-5996
30. Nordstrom DK. (2000). Advances in the hydrogeochemistry and microbiology of Acid Mine Waters. Int Geol Rev 42: 499-515
31. Okabe S, Kindaichi T, Ito T. (2004). MAR-FISH-An ecophisiological approach to link phylogenetic affiliation and in situ metabolic activity of microorganisms at a single-cell resolution. Microb Environ 19: 83-98
32. Pernthaler A, Pernthaler J, Amann R. (2004). Sensitive multi-color fluorescence in situ hybridisation for the identification of environmental microorganisms. Mol Microb Ecol Man Second Ed 3: 711-726
33. Pronk JT, Johnson DB. (1992). Oxidation and reduction of iron by acidophilic Bacteria. Geomicrobiol J 10: 153-171
34. Reinhardt H, Kriews M, Miller H, Schrems O, Ludke C, Hoffmann E et al. (2001). Laser ablation inductively coupled plasma mass spectrometry: A new tool for trace element analysis in ice cores. Fresenius J Anal Chem 370: 629-636
35. Rogers AW. (1979). Techniques of Autoradiography. Elsevier: New York, NY, USA
36. Rowe OF, Sanchez-Espana J, Hallberg KB, Johnson DB. (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
37. Singer PC, Stumm W. (1970). Acidic mine drainage: The rate-determining step. Science 167: 1121-1123
38. Steedman HF. (1957). Polyester wax; a new ribboning embedding medium for histology. Nature 179: 1345
39. Stookey LL. (1970). Ferrozine-A new spectrophotometric reagent for iron. Anal Chem 42: 779-781
40. White RH, Zhou D. (1993). Biosynthesis of conenzymes in methanogens. In: Methanogenesis GJFerry (ed) Chapman and Hall: New York, NY, USA
41. Zakrzewski M, Bekel T, Ander C, Pühler A, Rupp O, Stoye J et al. (2012). MetaSAMS-A novel software platform for taxonomic classification, functional annotation and comparative analysis of metagenome datasets. J Biotechnol; e-pub ahead of print 29 September 2012; doi: 10.1016/j.jbiotec.2012. 09.013
42. Ziegler S, Ackermann S, Majzlan J, Gescher J. (2009). Matrix composition and community structure analysis of a novel bacterial pyrite leaching community. Environ Microbiol 11: 2329-2338
43. Zielinski FU, Pernthaler A, Duperron S, Raggi L, Giere O, Borowski C et al. (2009). Widespread occurrence of an intranuclear bacterial parasite in vent and seep bathymodiolin mussels. Environ Microbiol 11: 1150-1167