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Manipulation of pyrite colonization and leaching by iron-oxidizing Acidithiobacillus species

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Abstract

In this study, the process of pyrite colonization and leaching by three iron-oxidizing Acidithiobacillus species was investigated by fluorescence microscopy, bacterial attachment, and leaching assays. Within the first 4–5 days, only the biofilm subpopulation was responsible for pyrite dissolution. Pyrite-grown cells, in contrast to iron-grown cells, were able to oxidize iron(II) ions or pyrite after 24 h iron starvation and incubation with 1 mM H2O2, indicating that these cells were adapted to the presence of enhanced levels of reactive oxygen species (ROS), which are generated on metal sulfide surfaces. Acidithiobacillus ferrivorans SS3 and Acidithiobacillus ferrooxidans R1 showed enhanced pyrite colonization and biofilm formation compared to A. ferrooxidans T. A broad range of factors influencing the biofilm formation on pyrite were also identified, some of them were strain-specific. Cultivation at non-optimum growth temperatures or increased ionic strength led to a decreased colonization of pyrite. The presence of iron(III) ions increased pyrite colonization, especially when pyrite-grown cells were used, while the addition of 20 mM copper(II) ions resulted in reduced biofilm formation on pyrite. This observation correlated with a different extracellular polymeric substance (EPS) composition of copper-exposed cells. Interestingly, the addition of 1 mM sodium glucuronate in combination with iron(III) ions led to a 5-fold and 7-fold increased cell attachment after 1 and 8 days of incubation, respectively, in A. ferrooxidans T. In addition, sodium glucuronate addition enhanced pyrite dissolution by 25 %.

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References

  • Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42

    Google Scholar 

  • Amouric A, Brochier-Armanet C, Johnson DB, Bonnefoy V, Hallberg KB (2011) Phylogenetic and genetic variation among Fe(II)-oxidizing acidithiobacilli supports the view that these comprise multiple species with different ferrous iron oxidation pathways. Microbiology 157:111–122

    Article  CAS  PubMed  Google Scholar 

  • Barahona S, Dorador C, Zhang R, Aguilar P, Sand W, Vera M, Remonsellez F (2014) Isolation and characterization of a novel Acidithiobacillus ferrivorans strain from the Chilean Altiplano: attachment and biofilm formation on pyrite at low temperature. Res Microbiol. doi:10.1016/j.resmic.2014.07.015

  • Barreto M, Gehrke T, Harneit K, Sand W, Jedlicki E, Holmes D (2005) Unexpected insights into biofilm formation by Acidithiobacillus ferrooxidans revealed by genome analysis and experimental approaches. In: Harrison STL, Rawlings DE, Petersen J (Eds) Proceedings of the 16th International Biohydrometallurgy Symposium Compress, Cape Town, pp 817-825

  • Bellenberg S, Diaz M, Noel N, Sand W, Poetsch A, Guiliani N, Vera M (2014) Biofilm formation, communication and interactions of leaching bacteria during colonization of pyrite and sulfur surfaces. Res Microbiol. doi:10.1016/j.resmic.2014.08.006

  • Bellenberg S, Leon-Morales CF, Sand W, Vera M (2012) Visualization of capsular polysaccharide induction in Acidithiobacillus ferrooxidans. Hydrometallurgy 129–130:82–89

    Article  Google Scholar 

  • Bellenberg S, Vera M, Sand W (2011) Transcriptomic studies of capsular polysaccharide export systems involved in biofilm formation by Acidithiobacillus ferrooxidans. In: Qui G, Jiang T, Qin W, Liu X, Yang Y, Wang H (eds) Biohydrometallurgy: biotech key to unlock mineral resources value proceedings of the 19th International Biohydrometallurgy Symposium Central South University Press. Changsha, China, pp 362–365

    Google Scholar 

  • Borda MJ, Elsetinow AR, Schoonen MA, Strongin DR (2001) Pyrite-induced hydrogen peroxide formation as a driving force in the evolution of photosynthetic organisms on an early Earth. Astrobiology 1:283–288

    Article  CAS  PubMed  Google Scholar 

  • Brierley CL, Brierley JA (2013) Progress in bioleaching: part B: applications of microbial processes by the minerals industries. Appl Microbiol Biotechnol 97:7543–7552

    Article  CAS  PubMed  Google Scholar 

  • Chiume R, Minnaar SH, Ngoma IE, Bryan CG, Harrison STL (2012) Microbial colonisation in heaps for mineral bioleaching and the influence of irrigation rate. Miner Eng 39:156–164

    Article  CAS  Google Scholar 

  • DEV (1989) DIN 38 406: Deutsche Einheitsverfahren zur Wasser-, Abwasser- und Schlammuntersuchung; Kationen (Gruppe E), Teil 1 Bestimmung von Eisen (E1), Normenausschuss Wasserwesen im DIN Deutsches Institut für Normierung eV: 22 Lieferung 1989

  • Farah C, Vera M, Morin D, Haras D, Jerez CA, Guiliani N (2005) Evidence for a functional quorum-sensing type AI-1 system in the extremophilic bacterium Acidithiobacillus ferrooxidans. Appl Environ Microbiol 71:7033–7040

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    CAS  PubMed  Google Scholar 

  • Freitas F, Alves VD, Torres CAV, Cruz M, Sousa I, Melo MJ, Ramos AM, Reis MAM (2011) Fucose-containing exopolysaccharide produced by the newly isolated Enterobacter strain A47 DSM 23139. Carbohyd Polym 83:159–165

    Article  CAS  Google Scholar 

  • Gehrke T, Telegdi J, Thierry D, Sand W (1998) Importance of extracellular polymeric substances from Thiobacillus ferrooxidans for bioleaching. Appl Environ Microbiol 64:2743–2747

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gonzalez A, Bellenberg S, Mamani S, Ruiz L, Echeverria A, Soulere L, Doutheau A, Demergasso C, Sand W, Queneau Y, Vera M, Guiliani N (2012) AHL signaling molecules with a large acyl chain enhance biofilm formation on sulfur and metal sulfides by the bioleaching bacterium Acidithiobacillus ferrooxidans. Appl Microbiol Biotechnol 97:3729–3737

    Article  PubMed  Google Scholar 

  • Hallberg KB, Gonzalez-Toril E, Johnson DB (2009) Acidithiobacillus ferrivorans, sp. nov.; facultatively anaerobic, psychrotolerant iron-, and sulfur-oxidizing acidophiles isolated from metal mine-impacted environments. Extremophiles 14:9–19

    Article  PubMed  Google Scholar 

  • Harneit K, Göksel A, Kock D, Klock JH, Gehrke T, Sand W (2006) Adhesion to metal sulphide surfaces by cells of Acidithiobacillus ferrooxidans, Acidithiobacillus thiooxidans and Leptospirillum ferrooxidans. Hydrometallurgy 83:245–254

    Article  CAS  Google Scholar 

  • Hedrich S, Johnson DB (2013) Acidithiobacillus ferridurans sp. nov., an acidophilic iron-, sulfur- and hydrogen-metabolizing chemolithotrophic gammaproteobacterium. Int J Syst Evol Microbiol 63:4018–4025

    Article  CAS  PubMed  Google Scholar 

  • Hickman JW, Tifrea DF, Harwood CS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102:14422–14427

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Imlay JA (2013) The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11:443–454

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Janczarek M (2011) Environmental signals and regulatory pathways that influence exopolysaccharide production in rhizobia. Int J Mol Sci 12:7898–7933

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jones GC, Corin KC, van Hille RP, Harrison STL (2011) The generation of toxic reactive oxygen species (ROS) from mechanically activated sulphide concentrates and its effect on thermophilic bioleaching. Miner Eng 24:1198–1208

    Article  CAS  Google Scholar 

  • Kelly DP, Wood AP (2000) Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int J Syst Evol Microbiol 50:511–516

    Article  PubMed  Google Scholar 

  • Kupka D, Rzhepishevska OI, Dopson M, Lindstrom EB, Karnachuk OV, Tuovinen OH (2007) Bacterial oxidation of ferrous iron at low temperatures. Biotechnol Bioeng 97:1470–1478

    Article  CAS  PubMed  Google Scholar 

  • Liljeqvist M, Valdes J, Holmes DS, Dopson M (2011) Draft genome of the psychrotolerant acidophile Acidithiobacillus ferrivorans SS3. J Bacteriol 193:4304–4305

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mackintosh M (1978) Nitrogen fixation by Thiobacillus ferrooxidans. J Gen Microbiol 105:215–218

    Article  CAS  Google Scholar 

  • Mangold S, Harneit K, Rohwerder T, Claus G, Sand W (2008) Novel combination of atomic force microscopy and epifluorescence microscopy for visualization of leaching bacteria on pyrite. Appl Environ Microbiol 74:410–415

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mills AL, Herman JS, Hornberger GM, Dejesus TH (1994) Effect of solution ionic strength and iron coatings on mineral grains on the sorption of bacterial cells to quartz sand. Appl Environ Microbiol 60:3300–3306

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moses CO, Nordstrom DK, Herman JS, Mills AL (1987) Aqueous pyrite oxidation by dissolved oxygen and by ferric iron. Geochim Cosmochim Acta 51:1561–1571

    Article  CAS  Google Scholar 

  • Navarro CA, Orellana LH, Mauriaca C, Jerez CA (2009) Transcriptional and functional studies of Acidithiobacillus ferrooxidans genes related to survival in the presence of copper. Appl Environ Microbiol 75:6102–6109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ng FM, Dawes EA (1973) Chemostat studies on the regulation of glucose metabolism in Pseudomonas aeruginosa by citrate. Biochem J 132:129–140

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nooshabadi AJ, Rao KH (2014) Formation of hydrogen peroxide by sulphide minerals. Hydrometallurgy 141:82–88

    Article  Google Scholar 

  • Rodriguez-Leiva M, Tributsch H (1988) Morphology of bacterial leaching patterns by Thiobacillus ferrooxidans on synthetic pyrite. Arch Microbiol 149:401–405

    Article  CAS  Google Scholar 

  • Rodriguez Y, Ballester A, Blazquez ML, Gonzalez F, Munoz JA (2003) New information on the pyrite bioleaching mechanism at low and high temperature. Hydrometallurgy 71:37–46

    Article  CAS  Google Scholar 

  • Rohwerder T, Gehrke T, Kinzler K, Sand W (2003) Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl Microbiol Biotechnol 63:239–248

    Article  CAS  PubMed  Google Scholar 

  • Ruiz LM, Castro M, Barriga A, Jerez CA, Guiliani N (2011) The extremophile Acidithiobacillus ferrooxidans possesses a c-di-GMP signalling pathway that could play a significant role during bioleaching of minerals. Lett Appl Microbiol 54:133–139

    Article  PubMed  Google Scholar 

  • Sand W, Jozsa PG, Kovacs ZM, Sasaran N, Schippers A (2007) Long-term evaluation of acid rock drainage mitigation measures in large lysimeters. J Geochem Explor 92:205–211

    Article  CAS  Google Scholar 

  • Sand W, Rohde K, Sobotke B, Zenneck C (1992) Evaluation of Leptospirillum ferrooxidans for Leaching. Appl Environ Microbiol 58:85–92

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schippers A, Rohwerder T, Sand W (1999) Intermediary sulfur compounds in pyrite oxidation: implications for bioleaching and biodepyritization of coal. Appl Microbiol Biotechnol 52:104–110

    Article  CAS  Google Scholar 

  • Shiers DW, Blight KR, Ralph DE (2005) Sodium sulphate and sodium chloride effects on batch culture of iron oxidising bacteria. Hydrometallurgy 80:75–82

    Article  CAS  Google Scholar 

  • Shrihari RK, Modak JM, Kumar R, Gandhi KS (1995) Dissolution of particles of pyrite mineral by direct attachment of Thiobacillus ferrooxidans. Hydrometallurgy 38:175–187

    Article  CAS  Google Scholar 

  • Solari JA, Huerta G, Escobar B, Vargas T, Badilla-Ohlbaum R, Rubio J (1992) Interfacial phenomena affecting the adhesion of Thiobacillus ferrooxidans to sulphide mineral surfaces. Colloid Surface 69:159–166

    Article  CAS  Google Scholar 

  • Talla E, Hedrich S, Mangenot S, Ji B, Johnson DB, Barbe V, Bonnefoy V (2014) Insights into the pathways of iron- and sulphur-oxidation, and biofilm formation from the chemolithotrophic acidophile Acidithiobacillus ferrivorans CF27. Res Microbiol doi:10.1016/j.resmic.2014.08.002

  • Tributsch H (2001) Direct versus indirect bioleaching. Hydrometallurgy 59:177–185

    Article  CAS  Google Scholar 

  • Tributsch H, Rojas-Chapana JA (2000) Metal sulfide semiconductor electrochemical mechanisms induced by bacterial activity. Electrochim Acta 45:4705–4716

    Article  CAS  Google Scholar 

  • Valdes J, Pedroso I, Quatrini R, Dodson RJ, Tettelin H, Blake R 2nd, Eisen JA, Holmes DS (2008) Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genomics 9:597

    Article  PubMed Central  PubMed  Google Scholar 

  • Vera M, Krok B, Bellenberg S, Sand W, Poetsch A (2013a) Shotgun proteomics study of early biofilm formation process of Acidithiobacillus ferrooxidans ATCC 23270 on pyrite. Proteomics 13:1133–1144

    Article  CAS  PubMed  Google Scholar 

  • Vera M, Schippers A, Sand W (2013b) Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation—part A. Appl Microbiol Biotechnol 97:7529–7541

    Article  CAS  PubMed  Google Scholar 

  • Vera M, Rohwerder T, Bellenberg S, Sand W, Denis Y, Bonnefoy V (2009) Characterization of biofilm formation by the acidophilic bioleaching bacterium Acidithiobacillus ferrooxidans by a microarray transcriptome analysis. Adv Mat Res 71–73:175–178

    Article  Google Scholar 

  • Whitfield C (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75:39–68

    Article  CAS  PubMed  Google Scholar 

  • Williams KP, Kelly DP (2013) Proposal for a new class within the phylum Proteobacteria, Acidithiobacillia classis nov., with the type order Acidithiobacillales, and emended description of the class Gammaproteobacteria. Int J Syst Evol Microbiol 63:2901–2906

    Article  CAS  PubMed  Google Scholar 

  • **a JL, Wu S, Zhang RY, Zhang CG, He H, Jiang HC, Nie ZY, Qiu GZ (2011) Effects of copper exposure on expression of glutathione-related genes in Acidithiobacillus ferrooxidans. Curr Microbiol 62:1460–1466

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors cordially acknowledge Dr. Mark Dopson (Centre for Ecology and Evolution in Microbial model Systems, Linnaeus University, Sweden) for providing A. ferrivorans SS3 and Dr. Sergey Rogalski (Institute of Bioorganic Chemistry and Petrochemistry of National Academy of Sciences of Ukraine, Kiew) for his support with FT-IR sample preparation and measurement. We express our special thanks to the Geology Department of the Universität Duisburg-Essen and Mark Schumann for his kind assistance in mineral processing. Financial support by the Bundesministerium für Bildung und Forschung (BMBF) for the bilateral German-Ukrainian cooperation project 01DK13006 is gratefully acknowledged.

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  1. Fakultät für Chemie, Biofilm Centre, Aquatische Biotechnologie, Universität Duisburg-Essen Universitätsstr 5, 45141, Essen, Germany

    Sören Bellenberg, Robert Barthen, Ruiyong Zhang, Wolfgang Sand & Mario Vera

  2. National Academy of Sciences of Ukraine, D.K. Zabolotny Institute of Microbiology and Virology, Zabolotnogo Str. 154, DO3680 MSP, Kiev, Ukraine

    Mariia Boretska

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  1. Sören Bellenberg
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Correspondence to Sören Bellenberg.

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Bellenberg, S., Barthen, R., Boretska, M. et al. Manipulation of pyrite colonization and leaching by iron-oxidizing Acidithiobacillus species. Appl Microbiol Biotechnol 99, 1435–1449 (2015). https://doi.org/10.1007/s00253-014-6180-y

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