Effects of multiple electron acceptors on microbial interactions in a hydrogen-based biofilm

Environmental Science and Technology

Volumn 47, Issue 13, 2013, Pages 7396-7403

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

^a ARIZONA STATE UNIVERSITY   (United States)

^b ZHEJIANG UNIVERSITY   (China)

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

Author keywords

[No Author keywords available]

Indexed keywords

DELIVERY CAPACITY; DENITRIFYING BACTERIA; ELECTRON ACCEPTOR; ELECTRON-ACCEPTING; MEMBRANE BIOFILM REACTOR; MICROBIAL INTERACTIONS; ORDERS OF MAGNITUDE; SULFATE REDUCING BACTERIA;

BACTERIA; BIOFILMS; DENITRIFICATION; ELECTRONS; GENES; INORGANIC COMPOUNDS; POLYMERASE CHAIN REACTION; SULFUR;

REDUCTION;

HYDROGEN; OXYGEN; SULFATE;

BACTERIUM; BIOASSAY; BIOFILM; CHLORITE; DOMINANCE; ELECTRON; HYDROGEN; MICROBIAL ACTIVITY; NITRATE; SULFATE;

ARTICLE; BACTERIAL GENE; BETAPROTEOBACTERIA; BIOFILM; COMMUNITY STRUCTURE; CONTROLLED STUDY; DENITRIFYING BACTERIUM; DESULFOVIBRIO; DNA EXTRACTION; ELECTRON; EPSILONPROTEOBACTERIA; GENE DOSAGE; MICROBIAL COMMUNITY; NONHUMAN; ORGANISMAL INTERACTION; PYROSEQUENCING; REDUCTION; STEADY STATE; SULFUR OXIDIZER;

BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIAL PROTEINS; BIOFILMS; BIOREACTORS; DNA, BACTERIAL; HYDROGEN; NITRATES; OXIDATION-REDUCTION; OXYGEN; PERCHLORATES; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SULFATES;

EID: 84880094665     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es401310j     Document Type: Article

References (59)

1. Martin, K. J. & Nerenberg, R. The membrane biofilm reactor (MBfR) for water and waster treatment: Principles, applications and recent developments. Bioresour. Technol. 2012, Mar, 3.
2. Rittmann, B. E. The membrane biofilm reactor is a versatile platform for water and wastewater treatment Environ. Eng. Res. 2007, 12, 157-175
3. 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
4. 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
5. 2 in a membrane biofilm reactor Biotechnol. Bioeng. 2012, 109, 2200-2210
6. Logan, B. E. Assessing the outlook for perchlorate-remediation Environ. Sci. Technol. 2001, 35, 482-487
7. Kengen, S. W. M.; Rikken, G. B.; Hagen, W. R.; Van Ginkel, C. G.; Stams, A. J. M. Purification and characterization of perchlorate reductase from the chlorate-respiring strain GR-1 J. Bacteriol. 1999, 181, 6706-6711
8. 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
9. Coates, J. D.; Achenbach, L. A. Microbial perchlorate reduction: Rocket-fuelled metabolism Nat. Revi. 2004, 2, 569-580
10. 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
11. Nerenberg, R.; Kawagoshi, Y.; Rittmann, B. E. Microbial ecology of a perchlorate-reducing, hydrogen-based membrane biofilm reactor Water Res. 2008, 42, 1151-1159
12. 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
13. Philippot, L. Denitrifying genes in bacterial and archaeal genomes. Biochim. Biophys. Acta 2002, 1557, 355-76
14. 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
15. 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
16. Nielsen, L. P.; Christensen, P. B.; Revsbech, N. P.; Sorensen, J. Denitrification and oxygen respiration in biofilms studied with a microsensor for nitrous oxide and oxygen Microb. Ecol. 1990, 19, 63-72
17. Carter, J. P.; Hsaio, Y. H.; Richardson, D. J. Soil and sediment bacteria capable of aerobic nitrate respiration Appl. Environ. Microbiol. 1995, 61, 2852-2858
18. United States Environmental Protection Agency, Sulfate in drinking water. http://water.epa.gov/drink/contaminants/unregulated/sulfate.cfm
19. 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. App. Microbiol. 1997, 20, 374-380
20. 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
21. Peck, H. H. The ATP-dependent reduction of sulfate with hydrogen in extracts of Desulfovibrio desulf uricans Proc. Natl. Acad. Sci. 1959, 45, 701-708
22. 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
23. Odom, J. M. Industrial and environmental concerns with sulfate-reducing bacteria ASM News. 1990, 56, 473-476
24. 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
25. Ontiveros-Valencia, A.; Ziv-El, M.; Zhao, H. P.; Feng, L.; Rittmann, B. E.; Krajmalnik-Brown, R. Interactions between nitrate-reducing and sulfate-reducing bacteria coexisting in a hydrogen-fed biofilm Environ. Sci. Technol. 2012, 46, 11289-11298
26. Lucassen, E. C. H. E. T.; Smolders, A. J. P.; Van der Salm, A. L.; Roelofs, J. G. M. High groundwater nitrate concentrations inhibit eutrophication of sulphate-rich freshwater wetlands Biogeochem. 2004, 67, 249-267
27. 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
28. Dilling, W.; Cypionka, H. Aerobic respiration in sulfate-reducing bacteria FEMS Microbiol. Lett. 1990, 71, 123-127
29. 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 1: Model development and numerical solution Environ. Sci. Technol. 2012, 46, 1598-1607
30. 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
31. United States Environmental Protection Agency, Monitored Natural Attenuation of Inorganic Contaminants in Ground Water. http://nepis.epa.gov/ Adobe/PDF/60000N76.pdf
32. 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
33. Rittmann, B. E.; McCarty, P. L. Environmental Biotechnology: Principles and Applications; McGraw-Hill Book Co: New York. 2001.
34. 2-based membrane biofilm reactors J. Membr. Sci. 2012, 407/408, 176-183
35. Tataurov, A. V.; You, Y.; Owczarzy, R. O. Predicting ultraviolet spectrum of single stranded and double strand deoxyribonucleic acids Biophys. Chem. 2007, 133, 66-70
36. 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
37. 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 SYBR Green for Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, Prevotella intermedia, tetQ gene and total bacteria FEMS Immunol. Med. Microbiol. 2003, 39, 81-86
38. 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
39. Philippot, L. Use of functional genes to quantify denitrifiers in the environment Biochem. Soc. Trans. 2006, 34, 101-103
40. 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
41. 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
42. 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.; Knight, 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
43. Edgar, R. C. Search and clustering orders of magnitude faster than blast Bioinformatics. 2010, 26, 2460-2461
44. 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
45. 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
46. 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
47. 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
48. Zhao, H. P.; Ontiveros-Valencia, A.; Tang, Y.; Kim, B. O.; Ilhan, Z. E.; Krajmalnik-Brown, R.; Rittmann, B. E. Using a two-stage hydrogen-based membrane biofilm reactor (MBfR) to achieve complete perchlorate reduction in the presence of nitrate and sulfate Environ. Sci. Technol. 2013, 47, 1565-1572
49. Smoot, M.; Ono, K.; Ruscheinski, J.; Wang, P. L.; Ideker, I. Cytoscape 2.8: New features for data integration and network visualization Bioinformatics. 2011, 27, 431-432
50. Shannon, P.; Markiel, A.; Ozie, O.; Baliga, N. S.; Wang, J. T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: A software environment for integrated models of biomolecular interaction networks Genome Res. 2003, 13, 2498-2504
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. Muyzer, G.; Stams, A. J. M. The ecology and biotechnology of sulphate-reducing bacteria Nat. Rev. 2008, 6, 441-454
53. Ontiveros-Valencia, A.; Ilhan, Z. E.; Kang, D. W.; Rittmann, B. Krajmalnik-Brown, Rosa. Phylogenetic analysis of nitrate- and sulfate-reducing bacteria in a hydrogen-fed biofilm FEMS Microb Ecol. 2013, 10.1111/1574-6941. 12107
54. Mohanakrishnan, J.; Wegener, K.; Barr, J.; Yuan, Z.; Schramm, A.; Louise Meyer, R. Dynamic microbial response of sulfidogenic wastewater biofilm to nitrate Appl. Environ. Biotechnol. 2011, 91, 1647-1657
55. Kodama, Y.; Watanabe, K. Sulfuricurvum kujiense gen. nov., sp nov., a facultatively anaerobic, chemolithoautotrophic, sulfur-oxidizing bacterium isolated from an underground crude-oil storage cavity Int. J. Syst. Evol. Microbiol. 2004, 54, 2297-2300
56. Achenbach, L. A.; Michaelidou, U.; Bruce, R. A.; Fryman, J.; Coates, J. D. Dechloromonas agitate gen. nov., sp. nov. and Dechlorosoma suillum gen. nov., sp. nov., two novel environmental dominant (per)chlorate reducing bacteria and their phylogenetic position Int. J. Syst. Evol. Microbiol. 2001, 51, 527-533
57. Sahu, A. K.; Conneely, T.; Nuesslein, K. R.; Ergas, S. J. Biological perchloreate reduction in packed bed reactors using elemental sulfur Environ. Sci. Technol. 2009, 43, 4466-4471
58. Liu, M. C.; Peck, H. D., Jr. The isolation of a hexaheme cytochrome from Desulfovibrio desulfuricans and its identification as a new type of nitrite reductase J. Biol. Chem. 1981, 256, 13159-13164
59. Bruce, R. A.; Achenbach, L. A.; Coates, J. D. Reduction of (per)chlorate by a novel organism isolated from paper mill waste Environ. Microbiol. 1999, 1, 319-329