Microbial community structure and function of Nitrobenzene reduction biocathode in response to carbon source switchover

Water Research

Volumn 54, Issue , 2014, Pages 137-148

  Liang, Bin ^a   Cheng, Haoyi ^b   Van Nostrand, Joy D ^c   Ma, Jincai ^c   Yu, Hao ^a   Kong, Deyong ^a   Liu, Wenzong ^b   Ren, Nanqi ^a   Wu, Liyou ^c   Wang, Aijie ^a,b   Lee, Duu Jong ^a,d   Zhou, Jizhong ^c,e,f  

^a HARBIN INSTITUTE OF TECHNOLOGY   (China)

^b RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^c UNIVERSITY OF OKLAHOMA   (United States)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e TSINGHUA UNIVERSITY   (China)

^f LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Biocathode; Carbon source switchover; Function; Microbial community structure; Nitrobenzene reduction

Indexed keywords

ANILINE; CARBON; CATHODES; ELECTRIC FIELDS; FUNCTIONS; GENES; GLUCOSE; MICROORGANISMS; RNA;

BIOCATHODES; BIOELECTROCHEMICAL REDUCTIONS; ELECTROCHEMICALLY ACTIVE BACTERIA; MICROBIAL COMMUNITIES; MICROBIAL COMMUNITY STRUCTURES; POTENTIAL CONDUCTIVITY; SELECTIVE TRANSFORMATION; SWITCHOVER;

NITROBENZENE;

ANILINE; AROMATIC AMINE; BICARBONATE; CYTOCHROME C; GLUCOSE; NITROBENZENE; RNA 16S;

BENZENE; BIOFILM; BIOTRANSFORMATION; COMMUNITY RESPONSE; COMMUNITY STRUCTURE; ELECTRODE; ELECTROKINESIS; GLUCOSE; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; ORGANIC NITROGEN COMPOUND; PHYLOGENETICS;

ACTINOBACTERIA; ALCALIGENACEAE; ARTICLE; BACTEROIDETES; BIOCATHODE COMMUNITY; BIOFILM; CARBON FIXATION; CARBON SOURCE; CARBON SOURCE SWITCHOVER; COMMUNITY STRUCTURE; CONDUCTANCE; CONTROLLED STUDY; ELECTRIC FIELD; ENERGY CONSERVATION; FIRMICUTES; GENE SEQUENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INOCULATION; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; PARACOCCUS; PHYLOGENY; PRIORITY JOURNAL; PROTEOBACTERIA; PSEUDOMONADACEAE; REDUCTION;

BIOCATHODE; CARBON SOURCE SWITCHOVER; FUNCTION; MICROBIAL COMMUNITY STRUCTURE; NITROBENZENE REDUCTION;

ANILINE COMPOUNDS; AUTOTROPHIC PROCESSES; BACTERIA; BASE SEQUENCE; BIOELECTRIC ENERGY SOURCES; BIOFILMS; CARBON; CARBON CYCLE; CLUSTER ANALYSIS; CYTOCHROME P-450 ENZYME SYSTEM; ELECTRIC CONDUCTIVITY; ELECTRODES; ELECTRONS; FIMBRIAE PROTEINS; GENES, BACTERIAL; GENETIC VARIATION; LINEAR MODELS; NITROBENZENES; OXIDATION-REDUCTION; PHYLOGENY; PRINCIPAL COMPONENT ANALYSIS; RNA, RIBOSOMAL, 16S;

EID: 84894298324     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2014.01.052     Document Type: Article

References (57)

1. Berg I.A., Kockelkorn D., Ramos-Vera W.H., Say R.F., Zarzycki J., Hugler M., Alber B.E., Fuchs G. Autotrophic carbon fixation in archaea. Nat. Rev. Microbiol. 2010, 8(6):447-460.
2. Bers K., Leroy B., Breugelmans P., Albers P., Lavigne R., Sorensen S.R., Aamand J., De Mot R., Wattiez R., Springael D. A novel hydrolase identified by genomic-proteomic analysis of phenylurea herbicide mineralization by Variovorax sp. strain SRS16. Appl. Environ. Microbiol. 2011, 77(24):8754-8764.
3. Bianco P., Haladjian J. Recent progress in the electrochemistry of c-type cytochromes. Biochimie 1994, 76(7):605-613.
4. Cai P.J., Xiao X., He Y.R., Li W.W., Yu L., Lam M.H.W., Yu H.Q. Involvement of c-type cytochrome CymA in the electron transfer of anaerobic nitrobenzene reduction by Shewanella oneidensis MR-1. Biochem. Eng. J. 2012, 68:227-230.
5. Caporaso J.G., Lauber C.L., Walters W.A., Berg-Lyons D., Huntley J., Fierer N., Owens S.M., Betley J., Fraser L., Bauer M., Gormley N., Gilbert J.A., Smith G., Knight R. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. Isme J. 2012, 6(8):1621-1624.
6. Clarke T.A., Edwards M.J., Gates A.J., Hall A., White G.F., Bradley J., Reardon C.L., Shi L., Beliaev A.S., Marshall M.J., Wang Z.M., Watmough N.J., Fredrickson J.K., Zachara J.M., Butt J.N., Richardson D.J. Structure of a bacterial cell surface decaheme electron conduit. Proc. Natl. Acad. Sci. USA 2011, 108(23):9384-9389.
7. Claus H., Perret N., Bausinger T., Fels G., Preuß J., König H. TNT transformation products are affected by the growth conditions of Raoultella terrigena. Biotechnol. Lett. 2006, 29(3):411-419.
8. Coursolle D., Gralnick J.A. Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol. Microbiol. 2010, 77(4):995-1008.
9. Fann Y.C., Metosh-Dickey C.A., Winston G.W., Sygula A., Rao D.N.R., Kadiiska M.B., Mason R.P. Enzymatic and nonenzymatic production of free radicals from the carcinogens 4-nitroquinoline N-oxide and 4-hydroxylaminoquinoline N-oxide. Chem. Res. Toxicol. 1999, 12(5):450-458.
10. Firer-Sherwood M., Pulcu G.S., Elliott S.J. Electrochemical interrogations of the Mtr cytochromes from Shewanella: opening a potential window. J. Biol. Inorg. Chem. 2008, 13(6):849-854.
11. Fitzgerald L.A., Petersen E.R., Ray R.I., Little B.J., Cooper C.J., Howard E.C., Ringeisen B.R., Biffinger J.C. Shewanella oneidensis MR-1 Msh pilin proteins are involved in extracellular electron transfer in microbial fuel cells. Process Biochem. 2012, 47(1):170-174.
12. Fuchs G. Alternative pathways of carbon dioxide fixation: Insights into the early evolution of life?. Annu. Rev. Microbiol. 2011, 65:631-658.
13. Giltner C.L., Nguyen Y., Burrows L.L. Type IV Pilin proteins: versatile molecular modules. Microbiol. Mol. Biol. Rev. 2012, 76(4):740-772.
14. Gorby Y.A., Yanina S., McLean J.S., Rosso K.M., Moyles D., Dohnalkova A., Beveridge T.J., Chang I.S., Kim B.H., Kim K.S., Culley D.E., Reed S.B., Romine M.F., Saffarini D.A., Hill E.A., Shi L., Elias D.A., Kennedy D.W., Pinchuk G., Watanabe K., Ishii S., Logan B., Nealson K.H., Fredrickson J.K. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc. Natl. Acad. Sci. USA 2006, 103(30):11358-11363.
15. Han J.I., Choi H.K., Lee S.W., Orwin P.M., Kim J., LaRoe S.L., Kim T.g., O'Neil J., Leadbetter J.R., Lee S.Y., Hur C.G., Spain J.C., Ovchinnikova G., Goodwin L., Han C. Complete genome sequence of the metabolically versatile plant growth-promoting endophyte Variovorax paradoxus S110. J. Bacteriol. 2010, 193(5):1183-1190.
16. Hasan K., Patil S.A., Górecki K., Leech D., Hägerhäll C., Gorton L. Electrochemical communication between heterotrophically grown Rhodobacter capsulatus with electrodes mediated by an osmium redox polymer. Bioelectrochemistry 2012, 93:30-36.
17. He Z., Van Nostrand J.D., Zhou J. Applications of functional gene microarrays for profiling microbial communities. Curr. Opin. Biotechnol. 2012, 23(3):460-466.
18. 2-producing microbial biocathode. Biotechnol. Bioeng. 2012, 109(3):657-664.
19. Ju K.S., Parales R.E. Nitroaromatic compounds, from synthesis to biodegradation. Microbiol. Mol. Biol. Rev. 2010, 74(2):250-272.
20. Koder R.L., Haynes C.A., Rodgers M.E., Rodgers D.W., Miller A.F. Flavin thermodynamics explain the oxygen insensitivity of enteric nitroreductases. Biochemistry 2002, 41(48):14197-14205.
21. Li Y., Li H. Type IV Pili of Acidithiobacillus ferrooxidans can transfer electrons from extracellular electron donors. J. Basic Microbiol. 2013, 53:1-6.
22. Liang B., Cheng H.Y., Kong D.Y., Gao S.H., Sun F., Cui D., Kong F.Y., Zhou A.J., Liu W.Z., Ren N.Q., Wu W.W., Wang A.J., Lee D.J. Accelerated reduction of chlorinated nitroaromatic antibiotic chloramphenicol by biocathode. Environ. Sci. Technol. 2013, 47(10):5353-5361.
23. Liu W., Wang A., Cheng S., Logan B.E., Yu H., Deng Y., Nostrand J.D., Wu L., He Z., Zhou J. Geochip-based functional gene analysis of anodophilic communities in microbial electrolysis cells under different operational modes. Environ. Sci. Technol. 2010, 44(19):7729-7735.
24. Logan B.E. Exoelectrogenic bacteria that power microbial fuel cells. Nat. Rev. Microbiol. 2009, 7(5):375-381.
25. Lovley D.R. Powering microbes with electricity: direct electron transfer from electrodes to microbes. Environ. Microbiol. Reports 2011, 3(1):27-35.
26. Lovley D.R. Electromicrobiology. Annu. Rev. Microbiol. 2012, 66:391-409.
27. Lovley D.R., Nevin K.P. Electrobiocommodities: powering microbial production of fuels and commodity chemicals from carbon dioxide with electricity. Curr. Opin. Biotechnol. 2013, 24(3):385-390.
28. 2 production from waste activated sludge. Water Res. 2012, 46(7):2425-2434.
29. Ma Y.F., Wu J.F., Wang S.Y., Jiang C.Y., Zhang Y., Qi S.W., Liu L., Zhao G.P., Liu S.J. Nucleotide sequence of plasmid pCNB1 from Comamonas strain CNB-1 reveals novel genetic organization and evolution for 4-chloronitrobenzene degradation. Appl. Environ. Microbiol. 2007, 73(14):4477-4483.
30. Malvankar N.S., Vargas M., Nevin K.P., Franks A.E., Leang C., Kim B.C., Inoue K., Mester T., Covalla S.F., Johnson J.P., Rotello V.M., Tuominen M.T., Lovley D.R. Tunable metallic-like conductivity in microbial nanowire networks. Nat. Nanotechnol. 2011, 6(9):573-579.
31. Marvin-Sikkema F.D., de Bont J.A. Degradation of nitroaromatic compounds by microorganisms. Appl. Microbiol. Biotechnol. 1994, 42(4):499-507.
32. McMillan D.G.G., Marritt S.J., Butt J.N., Jeuken L.J.C. Menaquinone-7 is specific cofactor in tetraheme quinol dehydrogenase CymA. J. Biol. Chem. 2012, 287(17):14215-14225.
33. Mu Y., Rozendal R.A., Rabaey K., Keller J. Nitrobenzene removal in bioelectrochemical systems. Environ. Sci. Technol. 2009, 43(22):8690-8695.
34. Peres C.M., Naveau H., Agathos S.N. Biodegradation of nitrobenzene by its simultaneous reduction into aniline and mineralization of the aniline formed. Appl. Microbiol. Biotechnol. 1998, 49(3):343-349.
35. Pfeffer C., Larsen S., Song J., Dong M.D., Besenbacher F., Meyer R.L., Kjeldsen K.U., Schreiber L., Gorby Y.A., El-Naggar M.Y., Leung K.M., Schramm A., Risgaard-Petersen N., Nielsen L.P. Filamentous bacteria transport electrons over centimetre distances. Nature 2012, 491(7423):218-221.
36. Pokkuluri P.R., Londer Y.Y., Duke N.E.C., Pessanha M., Yang X., Orshonsky V., Orshonsky L., Erickson J., Zagyanskiy Y., Salgueiro C.A., Schiffer M. Structure of a novel dodecaheme cytochrome c from Geobacter sulfurreducens reveals an extended 12 nm protein with interacting hemes. J. Struct. Biol. 2011, 174(1):223-233.
37. Rafii F., Wynne R., Heinze T.M., Paine D.D. Mechanism of metronidazole-resistance by isolates of nitroreductase-producing Enterococcus gallinarum and Enterococcus casseliflavus from the human intestinal tract. FEMS Microbiol. Lett. 2003, 225(2):195-200.
38. Reguera G., McCarthy K.D., Mehta T., Nicoll J.S., Tuominen M.T., Lovley D.R. Extracellular electron transfer via microbial nanowires. Nature 2005, 435(7045):1098-1101.
39. Richter K., Schicklberger M., Gescher J. Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration. Appl. Environ. Microbiol. 2012, 78(4):913-921.
40. Richter L.V., Sandler S.J., Weis R.M. Two isoforms of Geobacter sulfurreducens PilA have distinct roles in pilus biogenesis, cytochrome localization, extracellular electron transfer, and biofilm formation. J. Bacteriol. 2012, 194(10):2551-2563.
41. Roldan M.D., Perez-Reinado E., Castillo F., Moreno-Vivian C. Reduction of polynitroaromatic compounds: the bacterial nitroreductases. FEMS Microbiol. Rev. 2008, 32(3):474-500.
42. Rosenbaum M., Aulenta F., Villano M., Angenent L.T. Cathodes as electron donors for microbial metabolism: which extracellular electron transfer mechanisms are involved?. Bioresour. Technol. 2011, 102(1):324-333.
43. Ross D.E., Flynn J.M., Baron D.B., Gralnick J.A., Bond D.R. Towards electrosynthesis in Shewanella: energetics of reversing the Mtr pathway for reductive metabolism. PLoS One 2011, 6(2):e16649.
44. Sevrioukova I.F., Li H.Y., Zhang H., Peterson J.A., Poulos T.L. Structure of a cytochrome P450-redox partner electron-transfer complex. Proc. Natl. Acad. Sci. USA 1999, 96(5):1863-1868.
45. Shen J., Zhang Y., Xu X., Hua C., Sun X., Li J., Mu Y., Wang L. Role of molecular structure on bioelectrochemical reduction of mononitrophenols from wastewater. Water Res. 2013, 47(15):5511-5519.
46. Spain J.C. Biodegradation of nitroaromatic compounds. Annu. Rev. Microbiol. 1995, 49:523-555.
47. Su W., Zhang L., Li D., Zhan G., Qian J., Tao Y. Dissimilatory nitrate reduction by Pseudomonas alcaliphila with an electrode as the sole electron donor. Biotechnol. Bioeng. 2012, 109(11):2904-2910.
48. Vargas M., Malvankar N.S., Tremblay P.L., Leang C., Smith J.A., Patel P., Synoeyenbos-West O., Nevin K.P., Lovley D.R. Aromatic amino acids required for Pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. mBio 2013, 4(2):e00105-e00113.
49. Virdis B., Read S.T., Rabaey K., Rozendal R.A., Yuan Z., Keller J. Biofilm stratification during simultaneous nitrification and denitrification (SND) at a biocathode. Bioresour. Technol. 2011, 102(1):334-341.
50. Wang A.J., Cheng H.Y., Liang B., Ren N.Q., Cui D., Lin N., Kim B.H., Rabaey K. Efficient reduction of nitrobenzene to aniline with a biocatalyzed cathode. Environ. Sci. Technol. 2011, 45(23):10186-10193.
51. Wang A.J., Cui D., Cheng H.Y., Guo Y.Q., Kong F.Y., Ren N.Q., Wu W.M. A membrane-free, continuously feeding, single chamber up-flow biocatalyzed electrolysis reactor for nitrobenzene reduction. J. Hazard. Mater. 2012, 199-200:401-409.
52. Wrighton K.C., Virdis B., Clauwaert P., Read S.T., Daly R.A., Boon N., Piceno Y., Andersen G.L., Coates J.D., Rabaey K. Bacterial community structure corresponds to performance during cathodic nitrate reduction. Isme J. 2010, 4(11):1443-1455.
53. Xing D.F., Cheng S.A., Logan B.E., Regan J.M. Isolation of the exoelectrogenic denitrifying bacterium Comamonas denitrificans based on dilution to extinction. Appl. Microbiol. Biotechnol. 2010, 85(5):1575-1587.
54. Yanto Y., Hall M., Bommarius A.S. Nitroreductase from Salmonella typhimurium: characterization and catalytic activity. Org. Biomol. Chem. 2010, 8(8):1826-1832.
55. Zhang G.D., Zhao Q.L., Jiao Y., Wang K., Lee D.J., Ren N.Q. Biocathode microbial fuel cell for efficient electricity recovery from dairy manure. Biosens. Bioelectron. 2012, 31(1):537-543.
56. Zhang Y., Xie J., Liu M., Tian Z., He Z., van Nostrand J.D., Ren L., Zhou J., Yang M. Microbial community functional structure in response to antibiotics in pharmaceutical wastewater treatment systems. Water Res. 2013, 47(16):6298-6308.
57. Zhou J., Liu W., Deng Y., Jiang Y.H., Xue K., He Z., Van Nostrand J.D., Wu L., Yang Y., Wang A. Stochastic assembly leads to alternative communities with distinct functions in a bioreactor microbial community. mBio 2013, 4(2):e00584-12.