Journal of Soils and Sediments

, Volume 12, Issue 3, pp 354–365 | Cite as

Enhanced nitrate reduction and current generation by Bacillus sp. in the presence of iron oxides

SOILS, SEC 2 • GLOBAL CHANGE, ENVIRON RISK ASSESS, SUSTAINABLE LAND USE • RESEARCH ARTICLE
First Online:
Received:
Accepted:

Abstract

Purpose

Fe(III) has been reported as a strictly competitive electron acceptor with respect to other substrate reductions by dissimilatory Fe(III)-reducing bacteria (DIRB). However, the effect of Fe(III) oxides on the substrate reduction by other microorganisms remain unknown. The aims of this study were to investigate the effects of iron oxides on the nitrate reduction and current generation by Bacillus sp., in which the nitrate and carbon anodes served as soluble and insoluble electron acceptors, respectively.

Materials and methods

Microbial nitrate reduction by Bacillus sp. were conducted in batch cultures in the absence or presence of four chemically synthesized iron(III) oxyhydroxides [i.e., α-FeOOH, γ-FeOOH, α-Fe2O3, and γ-Fe2O3]. Anaerobic techniques were used throughout all the experiments. NO 3 − /NO 2 − was determined by ion chromatography, and NH 4 + was measured by spectrophotometry at 420 nm after a color reaction with Nessler’s reagent. For total Fe(II) determination, samples were extracted using 0.5 M HCl and tested by spectrophotometry at 510 nm, and Fe(II) analyses in NO 3 − containing samples were performed using a sequential extraction technique. Current generation was tested using a bioelectrochemical reactor that consisted of two identical chambers separated by a cation exchange membrane.

Results and discussion

The results showed that four iron oxides markedly enhanced the nitrate reduction and current generation by Bacillus sp. Nitrate reduction by the Fe(II) on the oxide surface was proven to take place, but with lower reduction rate than the direct microbial nitrate reduction by Bacillus sp. Al2O3 and TiO2, as control without Fe(II) formation, also enhanced the nitrate reduction and current generation. It was proposed that the electron may be transferred from Bacillus sp. to conduction band of iron oxides to the nitrate or anode, according to their redox potential ranking as outer membrane enzyme of microorganisms < conduction band of iron oxides < electron acceptors.

Conclusions

This study demonstrated that the presence of iron oxides can obviously enhance both the nitrate reduction and current generation by Bacillus sp., which was in contrast to the previous report with respect to the inhibition effect of Fe(III) on substrate reduction by DIRB. With respect to the semiconductive properties of iron oxides, their roles during the nitrate reduction and current generation were speculated as a conduction band of iron oxides mediating the electron transfer from Bacillus sp. to the nitrate and anode.

Keywords

Current generation Bacillus sp. Iron oxides Iron reduction Nitrate reduction Semiconductors 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

The authors would thank the National Natural Science Foundations of China (no. 40901114, 41025003, and 41101217), “973” Program (no. 2010CB134508), Excellent Young Scientist Foundation in Guangdong Academy of Sciences (2010), China Postdoctoral Science Foundation (no. 2011M501104), and Natural Science Foundation of Guangdong Province (no. S2011040001094) for financial support.

References

  1. Behrends T, Van Cappellen P (2005) Competition between enzymatic and abiotic reduction of uranium(VI) under iron reducing conditions. Chem Geol 220:315–327CrossRefGoogle Scholar
  2. Beller HR (2005) Anaerobic, Nitrate-dependent oxidation of U(IV) oxide minerals by the chemolithoautotrophic bacterium Thiobacillus denitrificans. Appl Environ Microbiol 71:2170–2174CrossRefGoogle Scholar
  3. Bond DR, Lovley DR (2003) Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69:1548–1555CrossRefGoogle Scholar
  4. Boone DR, Liu Y, Zhao ZJ, Balkwill DL, Drake GR, Stevens TO, Aldrich HC (1995) Bacillus infernus sp. nov., an Fe(III)- and Mn(IV)-reducing anaerobe from the deep terrestrial subsurface. Int J Syst Bacteriol 45:441–448CrossRefGoogle Scholar
  5. Borch T, Kretzschmar R, Kappler A, Cappellen PV, Ginder-Vogel M, Voegelin A, Campbell K (2010) Biogeochemical redox processes and their impact on contaminant dynamics. Environ Sci Technol 44:15–23CrossRefGoogle Scholar
  6. Cabello P, Roldan MD, Moreno-Vivian C (2004) Nitrate reduction and the nitrogen cycle in archaea. Microbiology 150:3527–3546CrossRefGoogle Scholar
  7. Cheng GJ, Li XH (2009) Bioreduction of chromium (VI) by Bacillus sp. isolated from soils of iron mineral area. Eur J Soil Biol 45:483–487CrossRefGoogle Scholar
  8. Choi Y, Song JY, Jung S, Kim S (2001) Optimization of the performance of microbial fuel cells containing alkalophilic Bacillus sp. J Microbiol Biotechnol 11:863–869Google Scholar
  9. Coby AJ, Picardal FW (2005) Inhibition of NO3− and NO2− by microbial Fe(III) reduction: evidence of a reaction between NO2- and cell surface-bound Fe2+. Appl Environ Microbiol 71:5267–5274CrossRefGoogle Scholar
  10. Cooper DC, Picardal FW, Schimmelmann A, Coby AJ (2003) Chemical and biological interactions during nitrate and goethite reduction by Shewanella putrefaciens 200. Appl Environ Microbiol 69:3517–3525CrossRefGoogle Scholar
  11. DiChristina TJ (1992) Effects of nitrate and nitrite on dissimilatory iron reduction by Shewanella putrefaciens 200. J Bacteriol 174:1891–1896Google Scholar
  12. Dou J, Ding A, Liu X, Du Y, Deng D, Wang J (2010) Anaerobic benzene biodegradation by a pure bacterial culture of Bacillus cereus under nitrate reducing conditions. J Environ Sci (China) 22:709–715CrossRefGoogle Scholar
  13. Espinosa-de-los-Monteros J, Martinez A, Valle F (2001) Metabolic profiles and aprE expression in anaerobic cultures of Bacillus subtilis using nitrate as terminal electron acceptor. Appl Microbiol Biotechnol 57:379–384CrossRefGoogle Scholar
  14. Finneran KT, Housewright MR, Lovley DR (2002) Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments. Environ Microbiol 4:510–516CrossRefGoogle Scholar
  15. Gonzalez PJ, Correia C, Moura I, Brondino CD, Moura JJG (2006) Bacterial nitrate reductases: molecular and biological aspects of nitrate reduction. J Inorg Biochem 100:1015–1023CrossRefGoogle Scholar
  16. Hansen HCB, Koch CB, Nancke-Krogh H, Borggaard OK, Sørensen J (1996) Abiotic nitrate reduction to ammonium: key role of green rust. Environ Sci Technol 30:2053–2056CrossRefGoogle Scholar
  17. Hernandez ME, Newman DK (2001) Extracellular electron transfer. Cell Mol Life Sci 58:1562–1571CrossRefGoogle Scholar
  18. Hoffmann MR, Martin ST, Choi W, Bahnemann BW (1995) Environmental applications of semiconductor photocatalysis. Chem Rev 95:69–96CrossRefGoogle Scholar
  19. Holmes DE, Bond DR, Lovley DR (2004) Electron transfer by Desulfobulbus propionicus to Fe(III) and graphite electrodes. Appl Environ Microbiol 70:1234–1237CrossRefGoogle Scholar
  20. Jørgensen CJ, Jacobsen OS, Elberling B, Aamand J (2009) Microbial oxidation of pyrite coupled to nitrate reduction in anoxic groundwater sediment. Environ Sci Technol 43:4851–4857CrossRefGoogle Scholar
  21. Kanso SW, Greene AC, Patel BKC (2002) Bacillus subterraneus sp. nov., an iron- and manganese-reducing bacterium from a deep subsurface Australian thermal aquifer. Int J Syst Evol Microbiol 52:869–874CrossRefGoogle Scholar
  22. Kim BH, Kim HJ, Hyum MS, Park DH (1999) Direct electrode reaction of an Fe(III)-reducing bacterium, Shewanella putrefaciens. J Microbiol Biotechnol 9:127–131Google Scholar
  23. Li XM, Zhou SG, Li FB, Wu CY, Zhuang L, Xu W, Liu L (2009) Fe(III) oxide reduction and carbon tetrachloride dechlorination by a newly isolated Klebsiella pneumoniae strain L17. J Appl Microbiol 106:130–139CrossRefGoogle Scholar
  24. Li FB, Li XM, Zhou SG, Zhuang L, Cao F, Huang DY, Xu W, Liu TX, Feng CH (2010) Enhanced reductive dechlorination of DDT in an anaerobic system of dissimilatory iron-reducing bacteria and iron oxide. Environ Pollut 158:1733–1740CrossRefGoogle Scholar
  25. Li XM, LiuTX LiFB, Zhang W, Zhou SG, Li YT (2011) Reduction of structural Fe(III) in oxyhydroxides by Shewanella decolorationis S12 and characterization of the surface properties of iron minerals. J Soils Sediments. doi: 10.1007/s11368-011-0433-5
  26. Liu TX, Li XM, Li FB, Zhang W, Chen MJ, Zhou SG (2011) Reduction of iron oxides by Klebsiella pneumoniae L17: kinetics and surface properties. Colloid Surface A 379:143–150CrossRefGoogle Scholar
  27. Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49:219–286CrossRefGoogle Scholar
  28. Mimica D, Zagal JH, Bedioui F (2001) Electroreduction of nitrite by hemin, myoglobin and hemoglobin in surfactant films. J Electroanal Chem 497:106–113CrossRefGoogle Scholar
  29. Moreno-Vivián C, Cabello P, Martínez-Luque M, Blasco R, Castillo F (1999) Prokaryotic nitrate reduction: Molecular properties and functional distinction among bacterial nitrate reductases. J Bacteriol 181:6573–6584Google Scholar
  30. Mori S, Ishii K, Hirakawa Y, Nakamura R, Hashimoto K (2011) In vivo participation of artificial porphyrins in electron-transport chains: electrochemical and spectroscopic analyses of microbial metabolism. Inorg Chem 50:2037–2039CrossRefGoogle Scholar
  31. Nakamura R, Ishii K, Hashimoto K (2009a) In vivo participation of artificial porphyrins in electron-transport chains: electrochemical and spectroscopic analyses of microbial metabolism. Angew Chem Int Ed 48:1606–1608CrossRefGoogle Scholar
  32. Nakamura R, Kai F, Okamoto A, Newton GJ, Hashimoto K (2009b) Self-constructed electrically conductive bacterial networks. Angew Chem Int Ed 44:508–511CrossRefGoogle Scholar
  33. Nevin KP, Finneran KT, Lovley DR (2003) Microorganisms associated with uranium bioremediation in a high-salinity subsurface sediment. Appl Environ Microbial 69:3672–3675CrossRefGoogle Scholar
  34. Nimje VR, Chen CY, Chen CC, Jean JS, Reddy AS, Fan CW, Pan KY, Liu HT, Chen JL (2009) Stable and high energy generation by a strain of Bacillus subtilis in a microbial fuel cell. J Power Sources 190:258–263CrossRefGoogle Scholar
  35. Obare SO, Ito T, Balfour MH, Meyer GJ (2003) Ferrous hemin oxidation by organic halides at nanocrystalline TiO2 interfaces. Nano Lett 3:1151–1153CrossRefGoogle Scholar
  36. Obuekwe CO, Westlake DWS (1982) Effect of reducible compounds (potential electron acceptors) on reduction of ferric iron by Pseudomonas species. Microbiol Lett 19:57–62Google Scholar
  37. Ottley CJ, Davison W, Edmunds WM (1997) Chemical catalysis of nitrate reduction by iron(II). Geochim Cosmochim Acta 61:1819–1828CrossRefGoogle Scholar
  38. Paul T, Miller PL, Strathmann TJ (2007) Visible-light-mediated TiO2 photocatalysis of fluoroquinolone antibacterial agents. Environ Sci Technol 41:4720–4727CrossRefGoogle Scholar
  39. Pollock J, Weber KA, Lack J, Achenbach LA, Mormile MR, Coates JD (2007) Alkaline iron(III) reduction by a novel alkaliphilic, halotolerant. Bacillus sp. isolated from salt flat sediments of Soap Lake. Appl Microbiol Biotechnol 77:927–934CrossRefGoogle Scholar
  40. Rabaey K, Verstraete W (2005) Microbial fuel cells: novel biotechnology for energy generation. Trend Biotechnol 23:291–298CrossRefGoogle Scholar
  41. Rajakumar S, Ayyasamy PM, Shanthi K, Thavamani P, Velmurugan P, Song YC, Lakshmanaperumalsamy P (2008) Nitrate removal efficiency of bacterial consortium (Pseudomonas sp. KW1 and Bacillus sp. YW4) in synthetic nitrate-rich water. J Hazard Mater 157:553–563CrossRefGoogle Scholar
  42. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101CrossRefGoogle Scholar
  43. Reiche M, Torburg G, Kusel K (2008) Competition of Fe(III) reduction and methanogenesis in an acidic fen. FEMS Microbiol Ecol 65:88–101CrossRefGoogle Scholar
  44. Shen XY, Zhang LM, Shen JP, Li LH, Yuan CL, He JZ (2010) Soil type determines the abundance and community structure of ammonia-oxidizing bacteria and archaea in flooded paddy soils. J Soils Sediments 10:1510–1516CrossRefGoogle Scholar
  45. Staniszewski A, Morris AJ, Ito T, Meyer GJ (2007) Conduction band mediated electron transfer across nanocrystalline TiO2 surfaces. J Phys Chem B 111:6822–6828CrossRefGoogle Scholar
  46. Straub KL, Benz M, Schink B, Widdel F (1996) Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl Environ Microbiol 62:1458–1460Google Scholar
  47. Stromberg JR, Wnuk JD, Pinlac RAF, Meyer GJ (2006) Multielectron transfer at heme-functionalized nanocrystalline TiO2 reductive dechlorination of DDT and CCl4 forms stable carbene compounds. Nano Lett 6:1284–1286CrossRefGoogle Scholar
  48. Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180Google Scholar
  49. Thygesen A, Poulsen FW, Min B, Angelidaki I, Thomsen AB (2009) The effect of different substrates and humic acid on power generation in microbial fuel cell operation. Biores Technol 100:1186–1191CrossRefGoogle Scholar
  50. Wang XG, Liu CS, Li XM, Li FB, Zhou SG (2008) Photodegradation of 2-mercaptobenzothiazole in the γ-Fe2O3/oxalate suspension under UVA light irradiation. J Hazard Mater 153:426–433CrossRefGoogle Scholar
  51. Wang XJ, Yang J, Chen XP, Sun GX, Zhu YG (2009) Phylogenetic diversity of dissimilatory ferric iron reducers in paddy soil of Hunan, South China. J Soils Sediments 9:568–577CrossRefGoogle Scholar
  52. Weber KA, Picardal FW, Roden EE (2001) Microbially catalyzed nitrate-dependent oxidation of biogenic solid-phase Fe(II) compounds. Environ Sci Technol 35:1644–1650CrossRefGoogle Scholar
  53. Weber KA, Urrutia MM, Churchill PF, Kukkadapu RK, Roden EE (2006) Anaerobic redox cycling of iron by freshwater sediment microorganisms. Environ Microbiol 8:100–113CrossRefGoogle Scholar
  54. Xia X, Cao XX, Liang P, Huang X, Yang SP, Zhao GG (2010) Electricity generation from glucose by a Klebsiella sp. in microbial fuel cells. Appl Microbiol Biotechnol 87:383–390CrossRefGoogle Scholar
  55. Xing SH, Chen CR, Zhou BQ, Zhang H, Nang ZM, Xu ZH (2010) Soil soluble organic nitrogen and microbial processes under adjacent coniferous and broadleaf plantation forests. J Soils Sediments 10:748–757CrossRefGoogle Scholar
  56. Xu Y, Schoonen MAA (2000) The absolute energy positions of conduction and valence bands of selected semiconducting minerals. Am Miner 85:543–556Google Scholar
  57. Yang L, Steefel CI, Marcus MA, Bargar JR (2010) Kinetics of Fe(II)-catalyzed transformation of 6-line ferrihydrite under anaerobic flow conditions. Environ Sci Technol 44:5469–5475CrossRefGoogle Scholar
  58. Zhang SH, Cai LL, Liu Y, Shi Y, Li W (2009) Effects of NO2− and NO3− on the Fe(III)EDTA reduction in a chemical absorption–biological reduction integrated NOx removal system. Appl Microbiol Biotechnol 82:557–563CrossRefGoogle Scholar
  59. Zhang YZ, Mo GQ, Li XW, Zhang WD, Zhang JQ, Ye JS, Huang XD, Yu CZ (2011) A graphene modified anode to improve the performance of microbial fuel cells. J Power Sources 196:5402–5407CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Guangzhou Institute of GeochemistryChinese Academy of SciencesGuangzhouPeople’s Republic China
  2. 2.Guangdong Key Laboratory of Agricultural Environment Pollution Integrated ControlGuangdong Institute of Eco-Environmental and Soil SciencesGuangzhouPeople’s Republic of China
  3. 3.College of Natural Resources and EnvironmentSouth China Agricultural UniversityGuangzhouPeople’s Republic of China
  4. 4.Graduate School of the Chinese Academy of SciencesBeijingPeople’s Republic of China

Personalised recommendations