Identification of the bacterial community involved in methane-dependent denitrification in activated sludge using DNA stable-isotope probing

FEMS Microbiology Ecology

Volumn 64, Issue 3, 2008, Pages 494-506

  Osaka, Toshifumi ^a   Ebie, Yoshitaka ^b   Tsuneda, Satoshi ^a   Inamori, Yuhei ^b  

^a WASEDA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE FOR ENVIRONMENTAL STUDIES   (Japan)

Author keywords

Aerobic methanotrophs; Carbon cycle; Methane dependent denitrification; Methylotrophic denitrifiers; Stable isotope probing

Indexed keywords

BACTERIAL PROTEIN; METHANE; NITRATE; PMOA PROTEIN; RNA 16S; STABLE ISOTOPE;

ACTIVATED SLUDGE; BACTERIUM; CARBON CYCLE; COEXISTENCE; DENITRIFICATION; DNA; IDENTIFICATION METHOD; METHANOTROPHY; MICROBIAL COMMUNITY; NITRATE; NUCLEIC ACID ANALYSIS; STABLE ISOTOPE; WASTEWATER;

ACTIVATED SLUDGE; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIUM CULTURE; CULTURE MEDIUM; DENITRIFICATION; DNA PROBE; ECOSYSTEM; GAMMAPROTEOBACTERIA; GENE TARGETING; HYPHOMICROBIACEAE; METHANOTROPHIC BACTERIUM; METHANOTROPHY; METHYLOCOCCACEAE; MICROBIAL COMMUNITY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM;

BACTERIA; BACTERIAL PROTEINS; BIODIVERSITY; DNA FINGERPRINTING; DNA PROBES; DNA, BACTERIAL; DNA, RIBOSOMAL; ECOSYSTEM; ISOTOPE LABELING; METHANE; MOLECULAR SEQUENCE DATA; NITROGEN; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SEWAGE;

BACTERIA (MICROORGANISMS); GAMMAPROTEOBACTERIA; HYPHOMICROBIACEAE; METHYLOCOCCACEAE;

EID: 43149098323     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2008.00473.x     Document Type: Article

References (61)

1. Akunna JC, Bizeau C Moletta R (1993) Nitrate and nitrite reductions with anaerobic sludge using various carbon sources: glucose, glycerol, acetic acid, lactic acid and methanol. Water Res 27 : 1303 1312.
2. Amann RI, Ludwig W Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59 : 143 169.
3. Amaral JA, Archambault C, Richards SR Knowles R (1995) Denitrification associated with groups I and II methanotrophs in a gradient enrichment system. FEMS Microbiol Ecol 18 : 289 298.
4. Bodrossy L, Stralis-Pavese N, Murrell JC, Radajewski S, Weilharter A Sessitsch A (2003) Development and validation of a diagnostic microbial microarray for methanotrophs. Environ Microbiol 5 : 566 582.
5. Cataldo DA, Haroon M, Schrader LE Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6 : 71 80.
6. Cebron A, Bodrossy L, Chen Y, Singer AC, Thompson IP, Prosser JI Murrell JC (2007) Identity of active methanotrophs in landfill cover soil as revealed by DNA-stable isotope probing. FEMS Microbiol Ecol 62 : 12 23.
7. Costa C, Dijkema C, Friedrich M, Garcia-Encina P, Fernandez-Polanco F Stams AJM (2000) Denitrification with methane as electron donor in oxygen-limited bioreactors. Appl Microbiol Biotechnol 53 : 754 762.
8. Costello AM Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65 : 5066 5074.
9. Davies T (1973) Isolation of bacteria capable of utilizing methane as a hydrogen donor in the process of denitrification. Water Res 7 : 575 579.
10. Dumont MG Murrell JC (2005) Stable isotope probing - linking microbial identity to function. Nat Rev Microbiol 3 : 499 504.
11. Ebina J, Tsutsui T Shirai T (1983) Simultaneous determination of total nitrogen and total phosphorus in water using peroxodisulfate oxidation. Water Res 17 : 1721 1726.
12. Eisentraeger A, Klag P, Vansbotter B, Heymann E Dott W (2001) Denitrification of groundwater with methane as sole hydrogen donor. Water Res 35 : 2261 2267.
13. Frette L, Gejlsbjerg B Westermann P (1997) Aerobic denitrifiers isolated from an alternating activated sludge system. FEMS Microbiol Ecol 24 : 363 370.
14. Ginige MP, Hugenholtz P, Daims H, Wagner M, Keller J Blackall LL (2004) Use of stable-isotope probing, full-cycle rRNA analysis, and fluorescence in situ hybridization-microautoradiography to study a methanol-fed denitrifying microbial community. Appl Environ Microbiol 70 : 588 596.
15. Ginige MP, Keller J Blackall LL (2005) Investigation of an acetate-fed denitrifying microbial community by stable isotope probing, full-cycle rRNA analysis, and fluorescent in situ hybridization-microautoradiography. Appl Environ Microbiol 71 : 8683 8691.
16. Hanson RS Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60 : 439 471.
17. Hanson RS Wattenberg EV (1991) Ecology of methylotrophic bacteria. Biology of Methylotrophs (Goldberg I Rokem JS, eds), pp. 325 348. Butterworth-Heinemann, Boston, MA.
18. 4 on presence and activity of the indigenous methanotrophic community in rice field soil. Environ Microbiol 2 : 666 679.
19. Holmes A, Costell A, Lidstrom M Murrell J (1995) Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett 132 : 203 208.
20. Horz H-P, Yimga MT Liesack W (2001) Detection of methanotroph diversity on roots of submerged rice plants by molecular retrieval of pmoA, mmoX, mxaF, and 16S rRNA and ribosomal DNA, including pmoA-based terminal restriction fragment length polymorphism profiling. Appl Environ Microbiol 67 : 4177 4185.
21. Jenkins O, Byrom D Jones D (1984) Taxonomic studies on some obligate methanol-utilizing bacteria. Microbial Growth on C1 Compounds (Crawford R Hanson R, eds), pp. 255 261. ASM Press, Washington, DC.
22. Knowles R (1982) Denitrification. Microbiol Rev 46 : 43 70.
23. Knowles R (2005) Denitrifiers associated with methanotrophs and their potential impact on the nitrogen cycle. Ecol Eng 24 : 441 446.
24. Lin JL, Radajewski S, Eshinimaev BT, Trotsenko YA, McDonald IR Murrell JC (2004) Molecular diversity of methanotrophs in Transbaikal soda lake sediments and identification of potential active populations by stable isotope probing. Environ Microbiol 6 : 1049 1060.
25. Lueders T, Manefield M Friedrich MW (2004a) Enhanced sensitivity of DNA- and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environ Microbiol 6 : 73 78.
26. Lueders T, Wagner B, Claus P Friedrich MW (2004b) Stable isotope probing of rRNA and DNA reveals a dynamic methylotroph community and trophic interactions with fungi and protozoa in oxic rice field soil. Environ Microbiol 6 : 60 72.
27. Lueders T, Kindler R, Miltner A, Friedrich MW Kaestner M (2006) Identification of bacterial micropredators distinctively active in a soil microbial food web. Appl Environ Microbiol 72 : 5342 5348.
28. Mechsner K, Hamer G Paolis A (1985) Denitrification with methanotrophic/methylotrophic bacterial association in the presence of oxygen. Site 1 : 135 213.
29. Meiberg JGM, Bruinenberg PM Harder W (1980) Effect of dissolved oxygen tension on the metabolism of methylated amines in Hyphomicrobium X in the absence and presence of nitrate: evidence for "aerobic" denitrification. J Gen Microbiol 120 : 453 463.
30. Mohanty SR, Bodelier PLE, Floris V Conrad R (2006) Differential effects and nitrogenous fertilizers on methane-consuming microbes in rice field and forest soils. Appl Environ Microbiol 72 : 1346 1354.
31. Murrell JC, McDonald IR Bourne DG (1998) Molecular methods for the study of methanotroph ecology. FEMS Microbiol Ecol 27 : 103 114.
32. Muyzer G, Teske A Wirsen CO (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164 : 165 172.
33. Nesterov AI, Ivanova TI, Ilchenko VY, Gayazov RR Mshenskii YN (1988) Protein and polysaccharide composition during growth of Methylomonas methanica under chemostat conditions. Sov Biotechnol 5 : 18 22.
34. Neufeld JD, Schafer H, Cox MJ, Boden R, McDonald IR Murrell JC (2007a) Stable-isotope probing implicates Methylophaga spp and novel Gammaproteobacteria in marine methanol and methylamine metabolism. ISME J 1 : 480 491.
35. Neufeld JD, Wagner M Murrell JC (2007b) Who eats what, where and when? Isotope labeling experiments are coming of age. ISME J 1 : 103 110.
36. Osaka T, Yoshie S, Tsuneda S, Hirata A, Iwami N Inamori Y (2006) Identification of acetate- or methanol-assimilating bacteria under nitrate-reducing conditions by stable-isotope probing. Microb Ecol 52 : 253 266.
37. Patureau D, Davison J, Bernet N Moletta R (1994) Denitrification under various aeration conditions in Comamonas sp., strain SGLY2. FEMS Microbiol Ecol 14 : 71 78.
38. Radajewski S, Ienson P, Parekh NR Murrell JC (2000) Stable-isotope probing as a tool in microbial ecology. Nature 403 : 646 649.
39. Radajewski S, Webster G, Reay DS, Morris SA, Ineson P, Nedwell DB, Prosser JI Murrell JC (2002) Identification of active methylotroph populations in an acidic forest soil by stable isotope probing. Microbiology 148 : 2331 2342.
40. Raghoebarsing AA, Pol A, Van de Pas-Schoonen KT et al 2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440 : 918 921.
41. Reichenbach H (1999) The ecology of the Myxobacteria. Environ Microbiol 1 : 15 21.
42. Rhee G Fuhs G (1978) Wastewater denitrification with one-carbon compounds as energy source. J WPCF 50 : 2111 2119.
43. Rittmann BE Langeland WE (1985) Simultaneous denitrification with nitrification in single-channel oxidation ditches. J Water Pollut Control Fed 57 : 300 308.
44. Robertson LA Kuenen JG (1984) Aerobic denitrification: a controversy revived. Arch Microbiol 139 : 351 354.
45. Saitou N Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 : 406 425.
46. Saralov AI, Krylova IN, Saralova EE Kusnetsov SI (1984) Distribution and species composition of methane-oxidizing bacteria in lake water. Microbiology 53 : 695 701.
47. Schramm A, Santegoeds CM, Nielsen HK, Ploug H, Wagner M, Pribyl M, Wanner J, Amann R de Beer D (1999) On the occurrence of anoxic microniches, denitrification, and sulfate reduction in aerated activated sludge. Appl Environ Microbiol 65 : 4189 4196.
48. Shimkets LJ, Dworkin M Reichenbach H (2005) The Myxobacteria. Prokaryotes, an Evolving Electronic Resource for the Microbiological Community, Release 3.91. Springer-Verlag, New York.
49. Sundh I, Bastviken D Tranvik LJ (2005) Abundance, activity, and community structure of pelagic methane-oxidizing bacteria in temperate lakes. Appl Environ Microbiol 71 : 6746 6752.
50. Takaya N, Catalan-Sakairi MAB, Sakaguchi Y, Kato I, Zhou Z Shoun H (2003) Aerobic denitrifying bacteria that produce low levels of nitrous oxide. Appl Environ Microbiol 69 : 3152 3157.
51. Thalasso F, Vallecillo A, Garcia-Encina P Fernandez-Polanco F (1997) The use of methane as a sole carbon source for wastewater denitrification. Water Res 31 : 55 60.
52. Thompson JD, Higgins DG Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequencing weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 : 4673 4680.
53. Urakami T Komagata K (1986) Emendation of Methylobacillus Yordy and Weaver 1977, a genus for methanol-utilizing bacteria. Int J Syst Bacteriol 36 : 502 511.
54. Wagner M Loy A (2002) Bacterial community composition and function in sewage treatment systems. Curr Opin Biotechnol 13 : 218 227.
55. Waki M, Tanaka Y, Osada T Suzuki K (2002) Effects of nitrite and ammonium on methane-dependent denitrification. Appl Microbiol Biotechnol 59 : 338 343.
56. Weatherburn MW (1967) Phenol-hypochlorite reaction for determination of ammonia. J Anal Chem 39 : 971 974.
57. Werner M Kayser R (1991) Denitrification with biogas as external carbon source. Water Sci Technol 23 : 701 708.
58. Yan T, Ye Q, Zhou J Zhang C (2006) Diversity of functional genes for methanotrophs in sediments associated with gas hydrates and hydrocarbon seeps in the Gulf of Mexico. FEMS Microbiol Ecol 57 : 251 259.
59. Ye RW Thomas SM (2000) Microbial nitrogen cycles: physiology, genomics and applications. Curr Opin Microbiol 4 : 307 312.
60. Zhao HW, Mavinic DS, Oldham WK Koch FA (1999) Water Res 33 : 961 970.
61. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61 : 533 616.