Abstract
We studied the effect of electron competition on chromate (Cr(VI)) reduction in a methane (CH4)-based membrane biofilm reactor (MBfR), since the reduction rate was usually limited by electron supply. A low surface loading of SO4 2− promoted Cr(VI) reduction. The Cr(VI) removal percentage increased from 60 to 70% when the SO4 2− loading increased from 0 to 4.7 mg SO4 2−/m2-d. After the SO4 2− loading decreased back to zero, the Cr(VI) removal further increased to 90%, suggesting that some sulfate-reducing bacteria (SRB) stayed in the reactor to reduce Cr(VI). However, a high surface loading of SO4 2− (26.6 mg SO4 2−/m2-d) significantly slowed down the Cr(VI) reduction to 40% removal, which was probably due to competition between Cr(VI) and SO4 2− reduction. Similarly, when 0.5 mg/L of Se(VI) was introduced into the MBfR, Cr(VI) removal percentage slightly decreased to 60% and then increased to 80% when input Se(VI) was removed again. The microbial community strongly depended on the loadings of Cr(VI) and SO4 2−. In the sulfate effect experiment, three genera were dominant. Based on the correlation between the abundances of the three genera and the loadings of Cr(VI) and SO4 2−, we conclude that Methylocystis, a type II methanotroph, reduced both Cr(VI) and sulfate, Meiothermus only reduced Cr(VI), and Ferruginibacter only reduced SO4 2−.
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References
Ackerley DF, Gonzalez CF, Blake R II, Keyhan M, Matin A (2004) Mechanism of chromate reduction by the Escherichia coli protein, NfsA, and the role of different chromate reductases in minimizing oxidative stress during chromate reduction. Environ Microbiol 6(8):851–860. https://doi.org/10.1111/j.1462-2920.2004.00639.x
Anderson RA, Kozlovsky AS (1985) Chromium uptake, absorption, and excretion of subjects consuming self-selected diets. Am J Clin Nutr 41:1117–1183
APHA (1998) Method 3500-Cr D: Standard methods for the examination of water and waste water. American Public Health Association
Arias YM, Tebo BM (2003) Cr(VI) reduction by sulfidogenic and nonsulfidogenic microbial consortia. Appl Environ Microbiol 69(3):1847–1853. https://doi.org/10.1128/AEM.69.3.1847-1853.2003
Barnhart J (1997) Occurrences, uses and properties of chromium. Regul Toxicol Pharmacol 26(1):S3–S7. https://doi.org/10.1006/rtph.1997.1132
Bebien M, Chauvin JP, Adriano JM, Grosse S, Vermeglio A (2001) Effect of selenite on growth and protein synthesis in the phototrophic bacterium Rhodobacter sphaeroides. Appl Environ Microbiol 67:4440–4447
Burton G A, Giddings TH, Debrine P, Fall R (1987) High incidence of selenite-resistant bacteria from a site polluted with selenium. Appl Environ Microbiol 53:185–188
Cetin D, Donmez S, Donmez G (2008) The treatment of textile wastewater including chromium(VI) and reactive dye by sulfate-reducing bacterial enrichment. J Environ Manag 88(1):76–82. https://doi.org/10.1016/j.jenvman.2007.01.019
Chardin, B.; Giudici-Orticoni, M. T.; Luca, G. D.; · Guigliarelli, B.; Bruschi, M. Hydrogenases in sulfate-reducing bacteria function as chromium reductase. Appl Microbiol Biotechnol 2003, 63, 315–321, 3, DOI: https://doi.org/10.1007/s00253-003-1390-8
Cheung KH, Gu JD (2007) Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: a review. Int Biodeterior Biodegrad 59(1):8–15. https://doi.org/10.1016/j.ibiod.2006.05.002
Cheung KH, Gu JD (2003) Reduction of chromate (CrO4 2–) by an enrichment consortium and an isolate of marine sulfate-reducing bacteria. Chemosphere 52(9):1523–1529. https://doi.org/10.1016/S0045-6535(03)00491-0
Dayan AD, Paine AJ (2001) Mechanisms of chromium toxicity, carcinogenicity and allergenicity: review of the literature from 1985 to 2000. Hum Exp Toxicol 20(9):439–451. https://doi.org/10.1191/096032701682693062
Dedysh SV, Belova SE, Bodelier PLE, Smirnova KV, Khmelenina VN, Chidthaisong A, Trotsenko YA, Liesack W, Dunfield PF (2007) Methylocystis heyeri sp. nov., a novel type II methanotrophic bacterium possessing ‘signature’ fatty acids of type I methanotrophs. Int J Syst Evol Microbiol 57(3):472–479. https://doi.org/10.1099/ijs.0.64623-0
Doran JW (1982) Microorganisms and the biological cycling of selenium. Adv Microb Ecol 6:1–32. https://doi.org/10.1007/978-1-4615-8318-9_1
Francis CA, Obraztsova AY, Tebo B (2000) Dissimilatory metal reduction by the facultative anaerobe Pantoea agglomerans SP1. Appl Environ Microbiol 66(2):543–548. https://doi.org/10.1128/AEM.66.2.543-548.2000
Fournier E, Adam-Guillermin C, Potin-Gautier M, Pannier F (2010) Selenate bioaccumulation and toxicity in Chlamydomonas reinhardtii: Influence of ambient sulphate ion concentration. Aquat Toxicol 97(1):51–57
Fujita M, Ike M, Nishimoto S, Takahashi K, Kashiwa M (1997) Isolation and characterization of a novel selenate-reducing bacterium, Bacillus sp. SF-1. J Ferment Bioeng 83(6):517–522. https://doi.org/10.1016/S0922-338X(97)81130-0
Hu BL, Shen LD, Lian X, Zhu Q, Liu S, Huang Q, He ZF, Geng S, Cheng DQ, Lou LP, Xu XY, Zheng P, He YF (2014) Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands. PNAS 111(12):4495–4500. https://doi.org/10.1073/pnas.1318393111
Huber H, Jannasch H, Rachel R, Fuchs T, Stetter KO (1997) Archaeoglobus venef icus sp. nov., a novel facultative chemolithoautotrophic hyperthermophilic sulfite reducer, isolate from abyssal black smokers. Syst App Microbiol 20:374–380
Kantar C, Cetin Z, Demiray H (2008) In situ stabilization of chromium (VI) in polluted soils using organic ligands: the role of galacturonic, glucuronic and alginic acids. J Hazard Mater 159(2-3):287–293. https://doi.org/10.1016/j.jhazmat.2008.02.022
Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol 63(1):311–334. https://doi.org/10.1146/annurev.micro.61.080706.093130
Lai CY, Zhong L, Zhang Y, Chen JX, Wen LL, Shi LD, Sun YP, Ma F, Rittmann BE, Zhou C, Tang Y, Zheng P, Zhao HP (2016a) Bio-reduction of chromate in a methane-based membrane biofilm reactor. Environ Sci Technol 50(11):5832–5839. https://doi.org/10.1021/acs.est.5b06177
Lai CY, Wen LL, Shi LD, Zhao KK, Wang YQ, Yang XE, Rittmann BE, Zhou C, Tang Y, Zheng P, Zhao HP (2016b) Selenate and nitrate bioreductions using methane as the electron donor in a membrane biofilm reactor. Environ Sci Technol 50(18):10179–10186. https://doi.org/10.1021/acs.est.6b02807
Lai CY, Yang X, Tang Y, Rittmann BE, Zhao HP (2014) Nitrate shaped selenate reducing microbial community in a hydrogen-based biofilm reactor. Environ Sci Technol 48:3395–3402
Lemly AD (1993) Teratogenic effects of selenium in natural populations of fresh water fish. Ecotoxicol Environ Saf 26(2):181–204
Lenz M, Enright AM, Flaherty VO, Aelst ACV, Lens PNL (2009) Bioaugmentation of UASB reactors with immobilized Sulfurospirillum barnesii for simultaneous selenate and nitrate removal. Appl Microbiol Biotechnol 83(2):377–388. https://doi.org/10.1007/s00253-009-1915-x
Lovely DR (1993) Dissimilatory metal reduction. Annu Rev Microbiol 47:263–290
Lovley DR, Phillips EJP (1994) Reduction of chromate by Desulfovibrio vulgaris and its C3 cytochrome. Appl Environ Microbiol 60(2):726–728
Lovley DR, Coates JD (1997) Bioremediation of metal contamination. Curr Opin Biotechnol 8(3):285–289. https://doi.org/10.1016/S0958-1669(97)80005-5
Lozupone C, Hamady M, Knight R (2006) UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinf 7(1):371–385. https://doi.org/10.1186/1471-2105-7-371
Luo YH, Chen R, Wen LL, Meng F, Zhang Y, Lai CY, Rittmann BE, Zhao HP, Zheng P (2015) Complete perchlorate reduction using methane as the sole electron donor and carbon source. Environ Sci Technol 49:2341–2349
Ma J, Kobayashi DY, Yee N (2009) Role of menaquinone biosynthesis genes in selenate reduction by Enterobacter cloacae SLD1a-1 and Escherichia coli K12. Environ Microbiol 11(1):149–158. https://doi.org/10.1111/j.1462-2920.2008.01749.x
McLean J, Beveridge TJ (2001) Chromate reduction by a pseudomonas isolated from a site contaminated with chromated copper arsenate. Appl Environ Microbiol 67(3):1076–1084. https://doi.org/10.1128/AEM.67.3.1076-1084.2001
Michel C, Brugna M, Aubert C, Bernadac A, Bruschi M (2001) Enzymatic reduction of chromate: comparative studies using sulfate-reducing bacteria. Appl Microbiol Biotechnol 55(1):95–100. https://doi.org/10.1007/s002530000467
Mori K, Kim H, Kakegawa T, Hanada S (2003) A novel lineage of sulphate-reducing microorganisms: Thermodesulfobiaceae fam. nov. Thermodesulfobium narugense, gen. nov., sp. nov. a new thermophilic isolate from a hot spring. Extremophiles 7(4):283–290. https://doi.org/10.1007/s00792-003-0320-0
Palmer CD, Wittbrodt PR (1991) Processes affecting the remediation of chromium-contaminant sites. Environ Health Persp 92:25–40. https://doi.org/10.1289/ehp.919225
Park CH, Keyhan M, Wielinga B, Fendorf S, Matin A (2000) Purification to homogeneity and characterization of a novel Pseudomonas putida chromate reductase. Appl Environ Microbiol 66(5):1788–1795. https://doi.org/10.1128/AEM.66.5.1788-1795.2000
Peck HD Jr (1959) The ATP-dependent reduction of sulfate with hydrogen in extracts of Desulfovibrio desulfuricans. Proc Natl Acad Sci U S A 45(5):701–708. https://doi.org/10.1073/pnas.45.5.701
Rauschenbach I, Narasingarao P, Haggblom MM (2010) Desulfurispirillum indicum sp. nov., a selenate- and selenite-respiring bacterium isolated from an estuarine canal. Int J Syst Evol Microbiol 61:654–658
Rikmann E, Zekker I, Tomingas M, Tenno T, Menert A, Loorits L, Tenno T (2012) Sulfate-reducing anaerobic ammonium oxidation as a potential treatment method for high nitrogen-content wastewater. Biodegradation 23(4):509–524. https://doi.org/10.1007/s10532-011-9529-2
Rittmann BE, McCarty PL (2001) Environmental biotechnology: principles and applications. McGraw-Hill Book Co, New York
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504. https://doi.org/10.1101/gr.1239303
Smith WL, Gadd GM (2000) Reduction and precipitation of chromate by mixed culture sulfate-reducing bacterial biofilms. J Appl Microbiol 88(6):983–991. https://doi.org/10.1046/j.1365-2672.2000.01066.x
Srivastava S, Prakash S, Srivastava MM (1999) Chromium mobilization and plant availability—the impact of organic complexing ligands. Plant Soil 212:203–208
Tang Y, Zhao HP, Marcus AK, Krajmalnik-Brown R, Rittmann BE (2012a) A steady-state biofilm model for simultaneous reduction of nitrate and perchlorate, part 1: model development and numerical solution. Environ Sci Technol 46(3):1598–1607. https://doi.org/10.1021/es203129s
Tang Y, Zhao HP, Marcus A, Krajmalnik-Brown R, Rittmann BE (2012b) A steady-state-biofilm model for simultaneous reduction of nitrate and perchlorate—part 2: parameter optimization and results and discussion. Environ Sci Technol 46(3):1608–1615. https://doi.org/10.1021/es203130r
Tang Y, Zhou C, Van Ginkel S, Ontiveros-Valencia A, Shin J, Rittmann BE (2012c) Hydrogen permeability of the hollow fibers used in H2-based membrane biofilm reactors. J Membrane Sci 407-408:176–183. https://doi.org/10.1016/j.memsci.2012.03.040
United States Environmental Protection Agency (2015) Appendix A to subpart O-regulated contaminants
Vatsouria A, Vainshtein M, Kuschk P, Wiessner ADK, Kaestner M (2005) Anaerobic co-reduction of chromate and nitrate by bacterial cultures of Staphylococcus epidermidis L-02. J Ind Microbiol Biotechnol 32:409–414
Waki M, Yasuda T, Yokoyama H, Dai Hanajima D, Ogino A, Suzuki K, Wang P-C, Mori T, Komori K, Sasatsu M, Toda K, Ohtake H (1989) Isolation and characterization of an Enterobacter cloacae strain that reduces hexavalent chromium under anaerobic conditions. Appl Environ Microbiol 55:1665–1669
Wang PC, Toda K, Ohtake H, Kusaka I, Yabe I (1991) Membrane bound respiratory system of Enterobacter cloacae strain HO1 grown anaerobically with chromate. FEMS Microbiol Lett 78(1):11–16. https://doi.org/10.1111/j.1574-6968.1991.tb04408.x
Yimga MT, Dunfield PF, Ricke P, Heyer J, Liesack W (2003) Wide distribution of a novel pmoA-like gene copy among type II methanotrophs, and its expression in Methylocystis strain SC2. Appl Environ Microbiol 69(9):5593–5602. https://doi.org/10.1128/AEM.69.9.5593-5602.2003
Zahoor A, Rehman A (2009) Isolation of Cr(VI) reducing bacteria from industrial effluents and their potential use in bioremediation of chromium containing wastewater. J Environ Sci 21(6):814–820. https://doi.org/10.1016/S1001-0742(08)62346-3
Zhao HP, Van Ginkel S, Kang DW, Rittmann BE, Krajmalnik-Brown R (2011) Interactions between perchlorate and nitrate reductions in the biofilm of a hydrogen-based membrane biofilm reactor. Environ Sci Technol 45(23):10155–10162. https://doi.org/10.1021/es202569b
Zhao HP, Ilhan ZE, Ontiveros-Valencia A, Tang Y, Rittmann BE, Krajmalnik-Brown R (2013) Effects of multiple electron acceptors on microbial interactions in a hydrogen-based biofilm. Environ. Sci. Technol. 47(13):7396–7403. https://doi.org/10.1021/es401310j
Zhao HP, Ontiveros-Valencia A, Tang Y, Kim B, Van-Ginkel S, Friese D, Overstreet R, Smith J, Evens P, Krajmalnik-Brown R, Rittmann BE (2014) Removal of multiple electron acceptors by pilot-scale, two-stage membrane biofilm reactors. Water Res 54:115–122
Zhong L, Lai CY, Shi LD, Wang KD, Dai YJ, Liu YW, Ma F, Rittmann BE, Zheng P, Zhao HP (2017) Nitrate effects on chromate reduction in a methane-based biofilm. Water Res 115:130–137. https://doi.org/10.1016/j.watres.2017.03.003
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The authors greatly thank the “Natural Science Funds for Distinguished Young Scholar of Zhejiang Province (LR17B070001),” the “Fundamental Research Funds for the Central Universities (2017XZZX010-03),” and the “National Natural Science Foundation of China (Grant No. 21377109, 21577123)” for their financial support.
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Lv, PL., Zhong, L., Dong, QY. et al. The effect of electron competition on chromate reduction using methane as electron donor. Environ Sci Pollut Res 25, 6609–6618 (2018). https://doi.org/10.1007/s11356-017-0937-7
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DOI: https://doi.org/10.1007/s11356-017-0937-7