Using a two-stage hydrogen-based membrane biofilm reactor (MBfR) to achieve complete perchlorate reduction in the presence of nitrate and sulfate

Environmental Science and Technology

Volumn 47, Issue 3, 2013, Pages 1565-1572

  Zhao, He Ping ^a,b   Ontiveros Valencia, Aura ^b   Tang, Youneng ^b,c   Kim, Bi O ^b   Ilhan, Zehra Esra ^b   Krajmalnik Brown, Rosa ^b   Rittmann, Bruce ^b  

^a ZHEJIANG UNIVERSITY   (China)

^b ARIZONA STATE UNIVERSITY   (United States)

^c University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROBIC BACTERIUM; DENITRIFYING BACTERIA; ENTEROBACTER; MEMBRANE BIOFILM REACTOR; MICROBIAL COMMUNITIES; PYROSEQUENCING; SURFACE LOADING;

BACTERIA; BIOREACTORS; DENITRIFICATION; GENES; HYDROGEN; INORGANIC COMPOUNDS; POLYMERASE CHAIN REACTION; REDUCTION;

LOADING;

NITRATE; PERCHLORATE; SULFATE;

BACTERIUM; BIOFILM; BIOREACTOR; CONCENTRATION (COMPOSITION); DENITRIFICATION; GENE EXPRESSION; HYDROGEN; MEMBRANE; MICROBIAL COMMUNITY; NITRATE; PERCHLORATE; POLLUTANT REMOVAL; SULFATE;

ANAEROBIC BACTERIUM; ARTICLE; BACTERIAL GENE; BIOFILM; BIOFILM REACTOR; CHEMICAL PARAMETERS; COMMUNITY STRUCTURE; CONCENTRATION (PARAMETERS); DECHLOROMONAS; DENITRIFICATION; DENITRIFYING BACTERIUM; ENTEROBACTER; FLOW RATE; HYDROGEN BASED MEMBRANE BIOFILM REACTOR; MICROBIAL COMMUNITY; NIRK GENE; NIRS GENE; NONHUMAN; PCRA GENE; PERCHLORATE REDUCING BACTERIUM; POLYMERASE CHAIN REACTION; PYROSEQUENCING; REACTION ANALYSIS; REDUCTION; RHODOBACTER; RHODOCYCLACEAE; RUBRIVIVAX; SPHAEROTILUS; SURFACE LOADING; WATER CONTAMINATION; WATER TREATMENT;

BACTERIA; BIODEGRADATION, ENVIRONMENTAL; BIOFILMS; BIOREACTORS; ELECTRONS; HYDROGEN; MEMBRANES, ARTIFICIAL; NITRATES; PERCHLORIC ACID; SULFATES;

EID: 84873429804     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es303823n     Document Type: Article

References (59)

1. Logan, B. E. Assessing the outlook for perchlorate-remediation Environ. Sci. Technol. 2001, 35, 482A-487A
2. United States Environmental Protection Agency. Fact Sheet: Final Regulatory Determination for Perchlorate, 2011. http://water.epa.gov/drink/ contaminants/unregulated/upload/FactSheet-PerchlorateDetermination.pdf.
3. Gu, B.; Coates, J. D. Perchlorate Environmental Occurrence: Interactions and Treatment; Springer: Boston, Maryland, U.S.A., 2006.
4. Van Ginkel, C. G.; Rikken, G. B.; Kroon, A. G. M.; Kengen, S. W. M. Purification and characterization of chlorite dismutase: a novel oxygen-generating enzyme Arch. Microbiol. 1996, 166, 321-326
5. Martin, K. J.; Nerenberg, R. The membrane biofilm reactor (MBfR) for water and wastewater treatment: Principles, applications and recent developments Bioresour. Technol. 2012, 122, 83-94
6. Zhao, H. P.; Van Ginkel, S.; Kang, D.-W.; Rittmann, B. E.; Krajmalnik-Brown, R. Interactions between perchlorate and nitrate reductions in the biofilm of a hydrogen-based membrane biofilm reactor Environ. Sci. Technol. 2011, 45, 10155-10162
7. Rittmann, B. E. The membrane biofilm reactor is a versatile platform for water and wastewater treatment Environ. Eng. Res. 2007, 12, 157-175
8. Rittmann, B. E.; Nerenberg, R.; Lee, K. C.; Najm, I.; Gillogy, T. E.; Lehman, G. E.; Adham, S. S. Hydrogen-based hollow-fiber membrane biofilm reactor (MBfR) for removing oxidized contaminants Water. Sci. Technol. 2004, 4, 127-133
9. Ziv-El, M.; Popat, S. C.; Cai, K.; Halden, R. U.; Krajmalnik-Brown, R.; Rittman, B. E. Managing methanogens and homoacetogens to promote reductive dechlorination of trichloroethene with direct delivery of H2 in a membrane biofilm reactor Biotechnol. Bioeng. 2012, 109, 2200-2210
10. Herman, D. C.; Frankenberger, W. T. Bacterial reduction of perchlorate and nitrate in water J. Environ. Qual. 1999, 28, 1018-1024
11. Choi, H.; Silverstein, J. Inhibition of perchlorate reduction by nitrate in a fixed biofilm reactor J. Hazard. Mater. 2008, 159, 440-445
12. Nerenberg, R.; Rittmann, B. E.; Najm, I. Perchlorate reduction in a hydrogen-based membrane-biofilm reactor J. Am. Water. Work. Assoc. 2002, 94, 103-114
13. United States Environmental Protection Agency. Sulfate indrinking water, 2012. http://water.epa.gov/drink/contaminants/unregulated/sulfate.cfm
14. Odom, J. M. Industrial and environmental concerns with sulfate-reducing bacteria ASM News 1990, 56, 473-476
15. Dalsgaard, T.; Bak, F. Nitrate reduction in a sulfate-reducing bacterium, Desulfovibrio desulfuricans, isolated from rice paddy soil: sulfide inhibition, kinetics, and regulation Appl. Environ. Microbiol. 1994, 60, 291-297
16. Uhlmann, D.; Paul, L. Causes and effects of "nitrate saturation" in phosphate-deficient water bodies Water. Sci. Technol. 1994, 30, 281-288
17. Kaster, K.M.; Grigoriyan, A.; Jenneman, G.; Voordouw, G. Effect of nitrate and nitrite on sulphide production by two thermophilic, sulphate-reducing enrichments from an oil field in the North Sea Appl. Microbiol. Biotechnol. 2007, 75, 195-203
18. Hubert, C.; Voordouw, G. Oil field souring control by nitrate-reducing Sulphurospirillum spp. that outcompete sulfate-reducing bacteria for organic electron donors Appl. Environ. Microbiol. 2007, 73, 2644-2652
19. Tang, Y. N.; Ziv-El, M.; Zhou, C.; Shin, J. H.; Ahn, C. H.; Meyer, K.; Candalaria, D.; Swaim, P.; Friese, D.; Overstreet, R.; Scott, R.; Rittmann, B. E. Bioreduction of nitrate in groundwater using a pilot-scale hydrogen-base membrane biofilm reactor Front. Environ. Sci. Eng. 2010, 4, 280-285
20. Ziv-El, M.; Rittmann, B. E. Systematic evaluation of nitrate and perchlorate bioreduction kinetics in groundwater using a hydrogen-based membrane biofilm reactor Water. Res. 2009, 43, 173-181
21. Chung, J.; Shin, S.; Oh, J. Influence of nitrate, sulfate and operational parameters on the bioreduction of perchlorate using an up-flow packed bed reactor at high salinity Environ. Technol. 2010, 31, 693-704
22. Philippot, L. Denitrifying genes in bacterial and archaeal genomes Biochim. Biophys. Acta 2002, 1557, 355-376
23. Richardson, D. J.; Berks, B. C.; Russell, D. A.; Spiro, S.; Taylor, C. J. Functional, biochemical and genetic diversity of prokaryotic nitrate reductase Cell. Mol. Life. Sci. 2001, 58, 165-178
24. Throbaeck, I. N.; Enwall, K.; Jarvis, A.; Hallin, S. Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE FEMS. Microbiol. Ecol. 2004, 49, 401-417
25. Coates, J. D.; Achenbach, L. A. Microbial perchlorate reduction: rocket-fuelled metabolism Nat. Rev. 2004, 2, 569-580
26. Nerenberg, R.; Kawagoshi, Y.; Rittmann, B. E. Microbial ecology of a perchlorate-reducing, hydrogen-based membrane biofilm reactor Water. Res. 2008, 42, 1151-1159
27. Xu, J.; Trimble, J. J.; Steinber, L.; Logan, B. E. Chlorate and nitrate reduction pathways are separately induced in the perchlorate-respiring bacterium Dechlorosoma sp. KJ and the chlorate-respiring bacterium Pseudomonas sp. PDA Water. Res. 2004, 38, 673-680
28. Nozawa-Inoue, M.; Jien, M.; Hamilton, N. S.; Stewart, V.; Scow, K. M.; Hristova, K. R. Quantitative detection of perchlorate-reducing bacteria by real-time PCR targeting the perchlorate reductase gene Appl. Environ. Microbiol. 2008, 74, 1941-1944
29. Huber, H.; Jannasch, H.; Rachel, R.; Fuchs, T.; Stetter, K. O. Archaeoglobus veneficus sp. nov., a novel facultative chemolithoautotrophic hyperthermophilic sulfite reducer, isolate from abyssal black smokers Syst. Appl. Microbiol. 1997, 20, 374-380
30. Mori, K.; Kim, H.; Kakegawa, T.; Hanada, S. 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. 2003, 7, 283-290
31. Peck, H. H. The ATP-dependent reduction of sulfate with hydrogen in extracts of Desulfovibrio desulfuricans Proc. Natl. Acad. Sci. U.S.A. 1959, 45, 701-708
32. Kondo, J.; Nedwell, D. B.; Purdy, K. J.; de Queiroz Silva, S. Detection and enumeration of sulphate-reducing bacteria in estuarine sediments by competitive PCR Geomicrobiol. J. 2004, 21, 145-157
33. Tang, Y.; Zhao, H. P.; Marcus, A.; Krajmalnik-Brown, R.; Rittmann, B. E. A steady-state-biofilm model for simultaneous reduction of nitrate and perchlorate -Part 2: Parameter optimization and results and discussion Environ. Sci. Technol. 2012, 46, 1608-1615
34. Ontiveros-Valencia, A.; Ziv-El, M.; Zhao, H. P.; Feng, L.; Krajmalnik-Brown, R.; Rittmann, B. E. Interactions between nitrate-reducing and sulfate-reducing bacteria coexisting in a hydrogen-fed biofilm Environ. Sci. Technol. 2012, 46, 11289-11298
35. Nerenberg, R.; Rittmann, B. E. Reduction of oxidized water contaminants with a hydrogen-based, hollow fiber membrane biofilm reactor Water. Sci. Technol. 2004, 49, 223-230
36. Rittmann, B. E.; McCarty, P. L. Environmental Biotechnology: Principles and Applications; McGraw-Hill Book, Co.: New York, 2001.
37. 2-based membrane biofilm reactors J. Membr. Sci. 2012, 407, 176-183
38. Braker, G.; Fesefeldt, A.; Witzel, K. P. Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples Appl. Environ. Microbiol. 1998, 64, 3769-3775
39. Maeda, H.; Fujimoto, C.; Haruki, Y.; Maeda, T.; Kokeguchi, S.; Petelin, M.; Arai, H.; Tanimoto, I.; Nishimura, F.; Takashiba, S. Quantitative real-time PCR using TaqMan and SYBY Green for Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, Prevotella intermedia, tetQ gene, and total bacteria FEMS. Immunol. Med. Microbiol. 2003, 39, 81-86
40. Coates, J. D.; Chakraborty, R.; Lack, J. G.; O'Connor, S. M.; Cole, K. A.; Bender, K. S.; Achenbach, L. A. Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas Nature 2001, 411, 1039-1043
41. Philippot, L. Use of functional genes to quantify denitrifiers in the environment Biochem. Soc. Trans. 2006, 34, 101-103
42. Fogel, G. B.; Collins, C. R.; Li, J.; Brunk, C. F. Prokaryotic genome size and ssu rDNA copy number: estimation of microbial relative abundance from a mixed population Microb. Ecol. 1999, 38, 93-113
43. Sun, Y.; Wolcott, R. D.; Dowd, S. E. Tag-encoded FLX amplicon pyrosequencing for the elucidation of microbial and functional gene diversity in any environment Methods Mol. Biol. 2011, 733, 129-141
44. Caporaso, J. G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F. D.; Costello, E. K.; Fierer, N.; Pena, A. G.; Goodrich, J. K.; Gordon, J. I.; Huttley, G. A.; Kelley, S. T.; Knights, D.; Koenig, J. E.; Ley, R. E.; Lozupone, C. A.; McDonald, D.; Muegge, B. D.; Pirrung, M.; Reeder, J.; Sevinsky, J. R.; Tumbaugh, P. J.; Walters, W. A.; Widmann, J.; Yatsunenko, T.; Zaneveld, J.; Knight, R. Qiime allows analysis of high-throughput community sequencing data Nat. Methods. 2010, 7, 335-336
45. Edgar, R. C. Search and clustering orders of magnitude faster than blast Bioinformatics. 2010, 26, 2460-2461
46. Pruesse, E.; Quast, C.; Knittel, K.; Fuchs, B. M.; Ludwig, W.; Peplies, J.; Gloeckner, F. O.; Silva A comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB Nucleic. Acids. Res. 2007, 35, 7188-7196
47. DeSantis, T. Z.; Hugenholtz, P.; Larsen, N.; Rojas, M.; Brodie, E. L.; Keller, K.; Huber, T.; Dalevi, D.; Hu, P.; Andersen, G. L. Greengenes, a chimera-checked 16s rDNA gene database and workbench compatible with arb Appl. Environ. Microbiol. 2006, 72, 5069-5072
48. Caporaso, J. G.; Bittinger, K.; Bushman, F. D.; DeSantis, T. Z.; Andersen, G. L.; Knight, R. Pynast: A flexible tool for aligning sequences to a template alignment Bioinformatics 2010, 26, 266-267
49. Haas, B. J.; Gevers, D.; Earl, A. M.; Feldgarden, M.; Ward, D. V.; Giannoukos, G.; Ciulla, D.; Tabbaa, D.; Highlander, S. K.; Sodergren, E.; Methe, B.; DeSantis, T. Z.; Petrosino, J. F.; Knight, R.; Birren, B. W. Human microbiome C: Chimeric 16s rRNA sequence formation and detection in sanger and 454-pyrosequenced pcr amplicons Genome. Res. 2011, 21, 494-504
50. Price, M. N.; Dehal, P. S.; Arkin, A. P. Fasttree: Computing large minimum evolution trees with profiles instead of a distance matrix Mol. Biol. Evol. 2009, 26, 1641-1650
51. Tang, Y.; Ontiveros-Valencia, A.; Feng, L.; Zhou, C.; Krajmalnik-Brown, R.; Rittmann, B. E. A biofilm model to understand the onset of sulfate reduction in denitrifying membrane biofilm reactors Biotechnol. Bioeng. 2012, 10.1002/bit.24755
52. Giblin, T.; Frankenberger, W. T. Perchlorate and nitrate reductase activity in the perchlorate-respiring bacterium Perclace Microbiol. Res. 2001, 156, 311-315
53. Nagashima, S.; Kamimura, A.; Shimizu, T.; Nakamura-Isaki, S.; Aono, E.; Sakamoto, K.; Ichikawa, N.; Nakazawa, H.; Sekine, M.; Yamazaki, S.; Fujita, N.; Shimada, K.; Hanada, S.; Nagashima, K. V. P. Complete genome sequence of phototrophic Betaproteobacterium rubrivivax gelatinosus il144 J. Bacteriol. 2012, 194, 3541-3542
54. Ivanova, N.; Daum, C.; Lang, E.; Abt, B.; Kopitz, M.; Saunders, E.; Lapidus, A.; Lucas, S.; DelRio, T. G.; Nolan, M.; Tice, H.; Copeland, A.; Cheng, J. F.; Chen, F.; Bruce, D.; Goodwin, L.; Pitluck, S.; Mavromatis, K.; Pati, A.; Mikhailova, N.; Chen, A.; Palaniappan, K.; Land, M.; Hauser, L.; Chang, Y. J.; Jeffries, C. D.; Detter, J. C.; Brettin, T.; Rohde, M.; Goeker, M.; Bristow, J.; Markowitz, V.; Eisen, J. A.; Hugenholtz, P.; Kyrpides, N. C.; Klenk, H. P. Complete genome sequence of Haliangium ochraceum type strain (smp-2(t)) Stand. Genomic. Sci. 2010, 2, 96-106
55. Gridneva, E. V.; Grabovich, M. Y.; Dubinina, G. A.; Chernousova, E. Y.; Akimov, V. N. Ecophysiology of lithotrophic sulfur-oxidizing Sphaerotilus species from sulfide springs in the northern caucasus Microbiology. 2009, 78, 89-97
56. Gridneva, E.; Chernousova, E.; Dubinina, G.; Akimov, V.; Kuever, J.; Detkova, E.; Grabovich, M. Taxonomic investigation of representatives of the genus Sphaerotilus: descriptions of Sphaerotilus montanus sp. nov., Sphaerotilus hippei sp. nov., Sphaerotilus natans subsp. natans subsp. nov. and Sphaerotilus natans subsp. sulfidivorans subsp. nov., and an emended description of the genus Sphaerotilus Int. J. Syst. Evol. Microbiol. 2011, 61, 916-925
57. Thrash, J. C.; Pollock, J.; Torok, T.; Coates, J. D. Description of the novel perchlorate-reducing bacteria Dechlorobacter hydrogenophilus gen. Nov., sp nov and Propionivibrio militaris, sp nov Appl. Microbiol. Biotechnol. 2010, 86, 335-343
58. Shrout, J. D.; Struckhoff, G. C.; Parkin, G. F.; Schnoor, J. L. Stimulation and molecular characterization of bacterial perchlorate degradation by plant-produced electron donors Environ. Sci. Technol. 2006, 40, 310-317
59. Roldan, M. D.; Reyes, F.; Moreno-Vivian, C.; Castillo, F. Chlorate and nitrate reduction in the phototropohic bacteria Rhodobacter capsulatus and Rhodobacter sphaeroides Curr. Microbiol. 1994, 29, 241-245