Stable Isotope Probing Techniques and Bioremediation

Eugene L. Madsen

doi:10.1128/9781555816896.ch9

Chapter 9 : Stable Isotope Probing Techniques and Bioremediation

Author: Eugene L. Madsen¹

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Department of Microbiology, Wing Hall, Cornell University, Ithaca, NY 14853-8101

Content Type: Monograph

Publication Year: 2011

Category: Environmental Microbiology; Applied and Industrial Microbiology

Book DOI: 10.1128/9781555816896

Chapter DOI: 10.1128/9781555816896.ch9

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Stable Isotope Probing Techniques and Bioremediation, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555816896/9781555815370_Chap09-1.gif /docserver/preview/fulltext/10.1128/9781555816896/9781555815370_Chap09-2.gif

Abstract:

This chapter summarizes the state of the art for applications of stable isotope probing (SIP) to bio-degradation and bioremediation research. SIP is one of the many emerging tools of inquiry used by environmental microbiologists. The goals of this chapter are to catalog and analyze trends exhibited by the majority of studies published to date that are pertinent to biodegradation and bioremediation. 14C-based phospholipid fatty acid (PLFA)-SIP showed chromatographic profiles related to but distinct from known type II methanotrophs. Using PLFA-SIP analyses, a variety of comparisons were made between forest, shrubland, and pasture soils; type II methanotrophs were dominant in forest and shrubland, while type I methanotrophs dominated pasture soil. When suitable probes are available, fluorescent in situ hybridization (FISH) is an effective means of microscopic identification of microorganisms and can be combined with techniques using radioactive and stable isotopes to identify metabolically active microorganisms. The combined microscopic approaches of FISH and secondary ion mass spectrometry (SIMS) have tremendous potential to aid investigations examining the roles of bacteria in biogeochemical processes and in the biodegradation of organic pollutants. SIP is a means toward the goal of improved pollution-control technology. In general, no single technique or piece of evidence is sufficient to advance the discipline of environmental microbiology. But SIP is inherently heuristic—results have the potential to create new information and hypotheses that can be tested and confirmed with multidisciplinary approaches.

Citation: Madsen E. 2011. Stable Isotope Probing Techniques and Bioremediation, p 165-201. In Murrell J, Whiteley A (ed), Stable Isotope Probing and Related Technologies. ASM Press, Washington, DC. doi: 10.1128/9781555816896.ch9

Key Concept Ranking

Environmental Microbiology: 0.74164635
Microbial Ecology: 0.738699
Restriction Fragment Length Polymorphism: 0.42399326
Denaturing Gradient Gel Electrophoresis: 0.42120385

0.74164635

Highlighted Text: Show | Hide

Full text loading...

Figures

Stable Isotope Probing Techniques and Bioremediation

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816896.ch09-1,webId=/content/author/10.1128/9781555816896.ch09-1,properties={foaf_givenname=Eugene L., foaf_name=Eugene L. Madsen, foaf_surname=Madsen, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555816896.ch09-aff1]]}]]

/content/10.1128/9781555816896.ch09.ch09fig01

FIGURE 1

Overview of SIP procedures. Biomarkers (nucleic acids are the example) from only a small subset of the microbial community become labeled.

10.1128/9781555816896/f0166-01_thmb.gif

10.1128/9781555816896/f0166-01.gif

FIGURE 1

Overview of SIP procedures. Biomarkers (nucleic acids are the example) from only a small subset of the microbial community become labeled.

References

/content/book/10.1128/9781555816896.ch09

1. Bastias, B. A.,, I. C. Anderson,, J. I. Rangel-Castro,, P. I. Parkin,, J. I. Prosser, and, J. W. G. Cairney. 2009. Influence of repeated prescribed burning on incorporation of 13C from cellulose by forest soil fungi as determined by RNA stable isotope probing. Soil Biol. Biochem. 41: 467– 472.

2. Bastida F.,, M. Rosell,, A. G. Franchini,, J. Siefert,, S. Finsterbusch,, N. Jehmlich, S. Jechalke,, M. von Bergen and, H. H. Richnow. 2010. Elucidating MTBE degradation in a mixed consortium using a multidisciplinary approach. FEMs Microbiol Ecol. 73: 370– 384.

3. Baytshtok, V.,, H. Lu,, H. Park,, S. Kim,, R. Yu, and, K. Chandran. 2009. Impact of varying electron donors on the molecular microbial ecology and biokinetics of methylotrophic denitrifying bacteria. Biotechnol. Bioeng. 102: 1527– 1536.

4. Baytshtok, V.,, S. Kim,, R. Yu,, H. Park, and, K. Chandran. 2008. Molecular and biokinetic characterization of methylotrophic denitrification using nitrate and nitrite as terminal electron acceptors. Water Sci. Technol. 58: 359– 365.

5. Boschker, H. T. S.,, W. de Graaf,, M. Köster,, L.-A. Meyer-Reil, and, T. E. Cappenberg. 2001. Bacterial populations and processes involved in acetate and propionate consumption in anoxic brackish sediment. FEMS Microbiol. Ecol. 35: 97– 103.

6. Boschker, H. T. S.,, S. C. Nold,, P. Wellsbury,, D. Bos,, W. de Graff,, R. Pel,, R. J. Parkes, and, T. E. Cappenberg. 1998. Direct linking of microbial populations to specific biogeochemical processes by 13C-labelling of biomarkers. Nature 392: 801– 805.

7. Bull, I. D.,, N. R. Parekh,, G. H. Hall,, P. Ineson, and, R. P. Evershed. 2000. Detection and classification of atmospheric methane oxidizing bacteria in soil. Nature 405: 175– 178.

8. Cebron, A.,, L. Bodrossy,, Y. Chen,, A. C. Singer,, I. P. Thompson,, J. I. Prosser, and, J. C. Murrell. 2007a. Identity of active methanotrophs in landfill cover soil as revealed by DNA-stable isotope probing. FEMS Microbiol. Ecol. 62: 12– 23.

9. Cebron, A.,, L. Bodrossy,, N. Stralis-Pavese,, A. C. Singer,, I. P. Thompson, and, J. C. Murrell. 2007b. Nutrient amendments in soil DNA stable isotope probing experiments reduce the observed methanotroph diversity. Appl. Environ. Microbiol. 73: 798– 807.

10. Chandra, S. 2005. Quantitative imaging of subcellular calcium stores in mammalian LLC-PK 1 epithelial cells undergoing mitosis by SIMS ion microscopy. Eur. Cell Biol. 84: 783– 797.

11. Chandra, S.,, G. Pumphrey,, J. M. Abraham, and, E. L. Madsen. 2008. Dynamic SIMS ion microscopy imaging of individual bacterial cells for studies of isotopically labeled molecules. Appl. Surf. Sci. 255: 247– 251.

12. Chandra, S.,, D. R. Smith, and, G. H. Morrison. 2000. Subcellular imaging by dynamic SIMS ion microscopy. Anal. Chem. 72: 104A– 114A.

13. Chang, Y-J.,, P. E. Long,, R. Geyer,, A. D. Peacock,, C. T. Resch,, K. Sublette,, S. Pfiffner,, A. Smithgall,, R. T. Anderson,, H. A. Vrionis,, J. R. Stephen,, R. Dayvault,, I. Ortiz-Bernad,, D. R. Lovley, and, D. C. White. 2005. Microbial incorporation of 13C-labeled acetate at the field scale: Detection of microbes responsible for reduction of U(VI). Environ. Sci. Technol. 39: 9039– 9048.

14. Chauhan, A., and, A. Ogram, 2006a. Fatty acid-oxidizing consortia along a nutrient gradient in the Florida Everglades. Appl. Environ. Microbiol. 72: 2400– 2406.

15. Chauhan, A., and, A. Ogram, 2006b. Phylogeny of acetate-utilizing microorganisms in soils along a nutrient gradient in the Florida Everglades. Appl. Environ. Microbiol. 72: 6837– 6840.

16. Chen, Y.,, M. G. Dumont,, J. D. Neufeld,, L. Brodrossy,, N. Stralis-Pavese,, N. P. McNamara,, N. Ostle,, M. J. I. Briones, and, J. C. Murrell. 2008. Revealing the uncultivated majority: combining DNA stable-isotope probing, multiple displacement amplification and metagenomic analyses of uncultivated Methylocystis in acidic peatlands. Environ. Microbiol. 10: 2609– 2622.

17. Cliff, J. B.,, D. J. Gaspar,, P. J. Bottomley, and, D. D. Myrold. 2002. Exploration of inorganic C and N assimilation by soil microbes with time-of-flight secondary ion mass spectrometry. Appl. Environ. Microbiol. 68: 4067– 4073.

18. Cliff, J. B.,, K. H. Jarman,, N. B. Valentine,, S. L. Golledge,, D. J. Gaspar,, D. S. Wunschel, and, K. L. Wahl. 2005. Differentiation of spores of Bacillus subtilis grown in different media by elemental characterization using time-of-flight secondary ion mass spectrometry. Appl. Environ. Microbiol. 71: 6524– 6530.

19. Cupples, A. M., and, G. K. Sims. 2007. Identification of in situ 2,4-dichlorophenoxyacetic acid-degrading soil microorganisms using DNA-stable isotope probing. Soil Biol. Biochem. 39: 232– 238.

20. Degelmann, D. M,, S. Kolb,, M. Dumont,, J. C Murrell, and, H. L. Drake. 2009. Enterobacteriaceae facilitate the anaerobic degradation of glucose by a forest soil. FEMS Microbiol. Ecol. 68: 312– 319.

21. Dekas, A. E.,, R. S. Poretsky, and, V. J. Orphan. 2009. Deep-sea Archaea fix and share nitrogen in methane-consuming microbial consortia. Science 326: 422– 426.

22. DeLong, E. F. 2005. Microbial community genomics in the ocean. Nature Rev. Microbiol. 3: 459– 469.

23. DeRito, C. M., and, E. L. Madsen. 2009. Stable isotope probing reveals Trichosporon yeast to be active in situ in soil phenol metabolism. ISME J. 3: 477– 485.

24. DeRito, C. M.,, G. M. Pumphrey, and, E. L. Madsen. 2005. Use of field-based stable isotope probing to identify adapted populations and track carbon flow through a phenol-degrading soil microbial community. Appl. Environ. Microbiol. 71: 7858– 7865.

25. DeSantis, T. Z.,, P. Hugenholtz,, N. Larsen,, M. Rojas,, E. L. Brodie,, K. Keller,, T. Huber,, D. Dalevi,, P. Hu, and, G. L. Andersen. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72: 5069– 5072.

26. Dumont, M. G., and, J. C. Murrell. 2005. Stable isotope probing—linking microbial identity to function. Nat. Rev. Microbiol. 3: 499– 504.

27. Dumont, M. G.,, S. M. Radajewski,, C. B. Miguez,, I. R. MacDonald, and, J. C. Murrell. 2006. Identification of a complete methane monooxygenase operon from soil by combining stable isotope probing and metagenomic analysis. Environ. Microbiol. 8: 1240– 1250.

28. Egert, M.,, A. A. de Graaf, A. maathuis, P. de Waard,, C. M. Plugge,, H. Smidt,, N. E. P. Deutz,, C. Dijkema,, W. M. De Vos, and, K. Venema. 2007. Identification of glucose-fermenting bacteria present in an in vitro model of the human intestine by RNA-stable isotope probing. FEMS Microbiol. Ecol. 60: 126– 135.

29. Falkowski, P. G.,, T. Fenchel, and, E. F. DeLong. 2008. The microbial engines that drive Earth’s bio-geochemical cycles. Science 320: 1034– 1039.

30. Frishman, D. 2007. Protein annotation at genomic scale: The current status. Chem Rev. 107: 3448– 3466

31. Friedrich, M. W. 2006. Stable isotope probing of DNA: Insights into the function of uncultivated microorganisms from isotopically labeled metagenomes. Curr. Opin. Biotechnol. 17: 59– 66.

32. Gallagher, E.,, L. McGuinness,, C. Phelps,, L. Y. Young, and, L. J. Kerkhof. 2005. 13C-carrier DNA shortens the incubation time needed to detect benzoate-utilizing denitrifying bacteria by stable-isotope probing. Appl. Environ. Microbiol. 71: 5192– 5196.

33. Geyer, R.,, A. D. Peacock,, A. Miltner,, H. H. Rich-now,, D. C. White,, K. L. Sublette, and, M. Kastner. 2005. In situ assessment of biodegradation potential using Biotraps amended with 13C-labeled benzene or toluene. Environ. Sci. Technol. 39: 4983– 4989.

34. Ginige, M. P.,, J. Keller, and, L. L. Blackall. 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.

35. Ginige, M. P.,, P. Hugenholtz,, H. Daims,, M. Wagner,, J. Keller, and, L. L. Blackall. 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.

36. Hamberger, A.,, M. A. Horn,, M. G. Dumont,, J. C Murrell, and, H. L. Drake. 2008. Anaerobic consumers of monosaccharides in a moderately acidic fen. Appl. Environ. Microbiol. 74: 3112– 3120.

37. Han, B.,, Y. Chen,, G. Abell,, H. Jiang,, L. Bodrossy,, J. G. Zhao,, J. C Murrell, and, X. H. Xing. 2009. Diversity and activity of methanotrophs in alkaline soil from a Chinese coal mine. FEMS Microbiol. Ecol. 70: 196– 207.

38. Hanson, J. R.,, J. L Macalady,, D. Harris, and, K. M. Scow. 1999. Linking toluene degradation with specific microbial populations in soil. Appl. Envir. Microbiol. 65: 5403– 5408.

39. Hatamoto, M.,, H. Imachi,, A. Ohashi, and, H. Harada. 2007b. Identification and cultivation of anaerobic, syntrophic long-chain fatty acid-degrading microbes from mesophilic and thermophilic methanogenic sludges. Appl. Environ. Microbiol. 73: 1332– 1340.

40. Hatamoto, M.,, H. Imachi,, Y. Yashiro,, A. Ohashi, and, H. Harada. 2007a. Diversity of anaerobic microorganisms involved in long-chain fatty acid degradation in methanogenic sludges as revealed by RNA-based stable isotope probing. Appl. Environ. Microbiol. 73: 4119– 4127.

41. Hatamoto, M.,, H. Imachi,, Y. Yashiro,, A. Ohashi, and, H. Harada. 2008. Detection of active butyrate-degrading microorganisms in methanogenic sludges by RNA-based stable isotope probing. Appl. Environ. Microbiol. 74: 3610– 3614.

42. Henckel, T.,, P. Roslev, and, R. Conrad, 2000. Effects of O 2 and CH 4 on presence and activity of the indigenous methanotrophic community in rice field soil. Environ. Microbiol. 2: 666– 679.

43. Herrmann A. M.,, P. L. Clode,, I. R. Fletcher,, N. Nunan,, E. A. Stockdale,, A. G. O’Donnell, and, D. V. Murphy. 2007. A novel method for the study of the biophysical interface in soils using nanoscale secondary ion mass spectrometry. Rapid Commun. Mass. Spectrom. 21: 29– 34.

44. Hori, T.,, M. Noll,, Y. Igarashi,, M. W. Friedrich, and, R. Conrad. 2007. Identification of acetate-assimilating microorganisms under methanogenic conditions in anoxic rice field soil by comparative stable isotope probing of RNA. Appl. Environ. Microbiol. 73: 101– 109.

45. Hori, T.,, Müller,, Y. Igarashi,, R. Conrad, and, M. W. Friedrich. 2009. Identification of iron-reducing microorganisms in anoxic rice paddy soil by 13C-acetate probing. ISME J. 4: 267– 278.

46. House, C. H. 2007. Linking taxonomy with environmental geochemistry and why it matters to the field of geobiology. Geobiology 5: 1– 3.

47. Huang, W. E.,, A. Ferguson,, A. C. Singer,, K. Lawson,, I. P. Thompson,, R. M. Kalin,, M. J. Larkin,, M. J. Bailey, and, A. S. Whiteley. 2009. Resolving genetic functions within microbial populations: In situ analyses using rRNA and mRNA stable isotope probing coupled with single-cell Raman-fluorescence in situ hybridization. Appl. Environ. Microbiol. 75: 234– 241.

48. Huang, W. E.,, R. I. Griffiths,, I. P. Thompson,, M. J. Bailey, and, A. S. Whiteley. 2004. Raman microscopic analysis of single microbial cells. Anal. Chem. 76: 4452– 4458.

49. Huang, W. E.,, K. Stoecker,, R. Griffiths,, L. New-bold,, H. Daims,, A. S. Whiteley, and, M. Wagner. 2007. Raman-FISH: combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function. Environ. Microbiol. 8: 1878– 1889.

50. Hutchens E.,, S. Radajewski,, M. G. Dumont,, I. R McDonald, and, J. C. Murrell. 2004. Analysis of methanotrophic bacteria in Movile Cave by stable isotope probing. Environ. Microbiol. 6: 111– 120.

51. Illman, W. A., and, P. J. J. Alvarez. 2009. Performance assessment of bioremediation and natural attenuation. Crit. Rev. Environ. Sci. Technol. 39: 209– 270.

52. Jehmlich, N.,, F. Schmidt,, M. Hartwich,, M. von Bergen,, H.-H. Richnow, and, C. Vogt. 2008b. Incorporation of carbon and nitrogen atoms into proteins measured by protein-based stable isotope probing (Protein-SIP). Rapid Commun. Mass Spectrom. 22: 2889– 2897.

53. Jehmlich, N.,, F. Schmidt,, M. von Bergen, H.-H. Richnow, and, C. Vogt. 2008a. Protein-based stable isotope probing (Protein-SIP) reveals active species within anoxic mixed cultures. ISME J. 2: 1122– 1133.

54. Jensen, S.,, J. D. Neufeld,, N.-K. Birkeland,, M. Hovland, and, J. C. Murrell. 2008. Methane assimilation and trophic interactions with marine Methylomicrobium in deep-water coral reef sediment off the coast of Norway. FEMS Microbiol. Ecol. 66: 320– 330.

55. Jeon, C.-O.,, W. Park,, P. Padmanabhan,, C. DeRito,, J. R. Snape, and, E. L. Madsen. 2003. Discovery of a novel bacterium with distinctive dioxygenase that is responsible for in situ biodegradation in a contaminated sediment. Proc. Natl. Acad. Sci. USA 100: 13591– 13596.

56. Johnsen, A. R.,, A. Winding,, U. Karlson, and, P. Roslev. 2002. Linking of microorganisms to phenanthrene metabolism in soil by analysis of 13C-labeled cell lipids. Appl. Environ. Microbiol. 68: 6106– 6113.

57. Jones, M. D.,, D. R. Singleton,, D. P. Carstensen,, S. N. Powell,, J. S. Swanson,, F. K. Pfaender, and, M. D. Aitken. 2008. Effect of incubation conditions on the enrichment of pyrene-degrading bacteria identified by stable-isotope probing in an aged, PAH-contaminated soil. Microbial Ecol. 56: 341– 349.

58. Kalyuzhnaya, M. G.,, A. Lapidus,, N. Ivanova,, A. C. Copeland,, A. C McHardy,, E. Szeto,, A. Salamov,, I. V. Grigoriev,, D. Suciu,, S. R. Levine,, V. M Markowitz,, I. Rigoutsos,, S. G. Tringe,, D. C. Bruce,, P. M. Richardson,, M. E. Lidstrom, and, L. Chistoserdova. 2008. High-resolution metagenomics targets specific functional types in complex microbial communities. Nat. Biotechnol. 26: 1029– 1034.

59. Kasai, Y.,, Y. Takahata,, M. Manefield, and, K. Watanabe. 2006. RNA-based stable isotope probing and isolation of anaerobic benzene-degrading bacteria from gasoline-contaminated groundwater. Appl. Environ. Microbiol. 72: 3586– 3592.

60. Kästner, M.,, A. Fischer,, I. Nijenhuis,, R. Geyer,, N. Stelzer,, P. Bombach,, C. C. Tebbe, and, H. H. Richnow. 2006. Assessment of microbial in situ activity in contaminated aquifers. Eng. Life. Sci. 6: 234– 251.

61. Knoblauch, C.,, U. Zimmermann,, M. Blumenberg,, W. Michaelis, and, E.-M. Pfeiffer. 2008. Methane turnover and temperature response of methane-oxidizing bacteria in permafrost-affected soils of northeast Siberia. Soil Biol. Biochem. 40: 3004– 3013.

62. Kunapuli, U.,, T. Lueders, and, R. U. Meckenstock. 2007. The use of stable isotope probing to identify key iron-reducing microorganisms involved in anaerobic benzene degradation. ISME J. 1: 643– 653.

63. Lear, G.,, B. Song,, A. G. Gault,, D. A. Polya, and, J. R. Lloyd. 2007. Molecular analysis of arsenate-reducing bacteria within Cambodian sediments following amendment with acetate. Appl. Environ. Microbiol. 73: 1041– 1048.

64. Lechene, C.,, F. Hillion,, G. McMahon,, D. Benson,, A. M. Kleinfield,, J. P. Kampf,, D. Distel,, Y. Luyten,, J. Bonventre,, D. Hentschel,, K. M. Park,, S. Ito,, M. Schwartz,, G. Benichou, and, G. Slodzian. 2006. High-resolution quantitative imaging of mammalian and bacterial cells using stable isotope mass spectrometry. J. Biol. 5: 20– 49.

65. Lee, N.,, P. H. Nielsen,, K. H. Andreasen,, S. J. Juretschko,, L. Nielsen,, K.-H. Schleifer, and, M. Wagner. 1999. Combination of fluorescent in situ hybridization and microautoradiography—a new tool for structure-function analyses in microbial ecology. Appl. Environ. Microbiol. 65: 1289– 1297.

66. Leigh, M. B.,, V. H. Pellizari,, O. Uhlik,, R. Sutka,, J. Rodrigues,, N. E. Ostrom,, J. Zhou, and, J. M. Tiedje. 2007. Biphenyl-utilizing bacteria and their functional genes in a pine root zone contaminated with polychlorinated biphenyls (PCBs). ISME J. 1: 134– 148.

67. Lerch, T. Z.,, M.-F. Dignac,, N. Nunan,, G. Bardoux,, E. Barriuso, and, A. Mariotti. 2009. Dynamics of soil microbial populations involved in 2,4-D bio-degradation revealed by FAMe-based stable isotope probing. Soil Biol. Biochem. 41: 77– 85.

68. Li, T,, T. D. Wu,, L. Mazéas,, L. Toffin,, J. L. Guerquin-Kern,, G. Leblon, and, T. Bouchez. 2008. Simultaneous analysis of microbial identity and function using NanoSIMS. Environ. Microbiol. 10: 580– 588.

69. Lin, J. L.,, S. Radajewski,, B. T. Eshinimaev,, Y. A. Trotsenko,, I. R McDonald, and, J. C. Murrell. 2004. Molecular diversity of methanotrophs in Transbaikal soda lake sediments and identification of potentially active populations by stable isotope probing. Environ. Microbiol. 6: 1049– 1060.

70. Liou, J. S.-C.,, C. M. DeRito, and, E. L. Madsen. 2008. Field-based and laboratory stable isotope probing surveys of the identities of both aerobic and anaerobic benzene-metabolizing microorganisms in freshwater sediment. Environ. Microbiol. 10: 1964– 1977.

71. Lueders, T.,, B. Pommerenke, and, M. W. Friedrich. 2004a. Stable-isotope probing of microorganisms thriving at thermodynamic limits: Syntrophic propionate oxidation in flooded soil. Appl. Environ. Microbiol. 70: 5778– 5786.

72. Lueders, T.,, B. Wagner,, P. Claus, and, M. W. Friedrich. 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.

73. Luo, C. L.,, S. G. Xie,, W. M. Sun,, X. D. Li, and, A. M. Cupples. 2009. Identification of a novel toluene-degrading bacterium from the candidate phylum TM7, as determined by DNA stable isotope probing. Appl. Environ. Microbiol. 75: 4644– 4647.

74. Madsen, E. L. 2005. Identifying microorganisms responsible for ecologically significant biogeochemical processes. Nat. Microbiol. Rev. 3: 439– 446.

75. Madsen, E. L. 2006. The use of stable isotope probing techniques in bioreactor and field studies on bioremediation. Curr. Opin. Biotechnol. 17: 92– 97.

76. Madsen, E. L. 2008. Environmental Microbiology: from Genomes to Biogeochemistry. Wiley/Blackwell, Malden, MA.

77. Mahmood S.,, G. I. Paton, and, J. I. Prosser. 2005. Cultivation-independent in situ molecular analysis of bacteria involved in degradation of pentachlorophe-nol in soil. Environ. Microbiol. 7: 1349– 1360.

78. Manefield, M.,, R. I. Griffiths,, M. J. Bailey, and, A. S. Whiteley. 2006. Stable isotope probing: a critique of its use in linking phylogeny and function, p. 205–216. In P. Nannipieri and, K. Smalla (ed.), Soil Biology, vol. 8, Nucleic Acids and Proteins in Soil. Springer, Berlin, Germany.

79. Manefield, M.,, R. I. Griffiths,, M. B. Leigh,, R. Fisher, and, A. S. Whiteley. 2005. Functional and compositional comparison of two activated sludge communities remediating coking effluent. Environ. Microbiol. 7: 715– 722.

80. Manefield, M.,, R. Griffiths,, N. P. McNamara,, D. Sleep,, N. Ostle, and, A. Whiteley. 2007. Insights into the fate of a 13C labelled phenol pulse for stable isotope probing (SIP) experiments. J. Microbiol. Meth. 69: 340– 344.

81. Manefield, M.,, A. S. Whiteley, and, M. J. Bailey. 2004b. RNA-based stable isotope probing—unambiguously identifying organisms responsible for industrial phenol remediation. Intl. Biodeterior. Bio-degrad. 53: 247.

82. Manefield, M.,, A. S. Whiteley, and, M. J. Bailey. 2004a. What can stable isotope probing do for bioremediation? Intl. Biodeterior. Biodegrad. 54: 163– 166.

83. Manefield, M.,, A. S. Whiteley,, R. I. Griffiths, and, M. J. Bailey. 2002. RNA stable isotope probing, a novel means of linking microbial community function to phylogeny. Appl. Environ. Microbiol. 68: 5367– 5373.

84. Manichaikul, A.,, L. Ghamsari,, E. F. Y. Hom,, C. Lin,, R. R. Murray,, R. L. Chang,, S. Balaji,, T. Hao,, Y. Shen,, A. K. Chavali,, I. Thiele,, X. Yang,, C. Fan,, E. Mello,, D. E. Hill,, M. Vidal,, K. Salehi-Ashtiani, and, J. A. Papin. 2009. Metabolic network analysis integrated with transcript verification of sequenced genomes. Nature Methods 6: 589– 592.

85. Meyer, R. L.,, A. M. Saunders, and, L. L. Blackall. 2006. Putative glycogen-accumulating organisms belonging to the Alphaproteobacteria identified through rRNA-based stable isotope probing. Microbiology 152: 419– 429.

86. Miller, L. G.,, K. L. Warner,, S. M. Baesman,, R. S. Oremland,, I. R McDonald,, S. Radajewski, and, J. C. Murrell. 2004. Degradation of methyl bromide and methyl chloride in soil microcosms: Use of stable C isotope fractionation and stable isotope probing to identify reactions and the responsible microorganisms. Geochim. Cosmochim. Acta. 68: 3271– 3283.

87. Miyatake, T.,, B. J. MacGregor, and, H. T. S. Boschker. 2009. Linking microbial community function to phylogeny of sulfate-reducing Deltaproteobacteria in marine sediments by combining stable isotope probing with magnetic-bead capture hybridization of 16S rRNA. Appl. Environ. Microbiol. 75: 4927– 4935.

88. Mohanty, S. R.,, P. L. E. Bodelier,, V. Floris, and, R. Conrad. 2006. Differential effects of nitrogenous fertilizers on methane-consuming microbes in rice field and forest soils. Appl. Environ. Microbiol. 72: 1346– 1354.

89. Monard, C.,, F. Binet, and, P. Vandenkoornhuyse, 2008. Short-term response of soil bacteria to carbon enrichment in different soil microsites. Appl. Environ. Microbiol. 74: 5589– 5592.

90. Moreau, J. W.,, P. K. Weber,, M. C. Martin,, B. Gilbert,, D. I. Hutcheon, and, J. F. Banfield. 2007. Extracellular proteins limit the dispersal of biogenic nanoparticles. Science 316: 1600– 1603.

91. Morris, S. A.,, S. Radajewski,, T. W. Willison, and, J. C. Murrell. 2002. Identification of the functionally active methanotroph population in a peat soil microcosm by stable-isotope probing. Appl. Environ. Microbiol. 68: 1446– 1453.

92. National Research Council. 2000. Natural Attenuation for Groundwater Remediation. National Academy Press, Washington, DC.

93. Nercessian, O.,, E. Noyes,, M. G. Kalyuzhnaya,, M. E. Lidstrom, and, L. Chistoserdova. 2005. Bacterial populations active in metabolism of C 1 compounds in the sediment of lake Washington, a freshwater lake. Appl. Environ. Microbiol. 71: 6885– 6899.

94. Neufeld, J. D.,, R. Boden,, H. Moussard,, H. Schaefer, and, J. C. Murrell. 2008. Substrate-specific clades of active marine methylotrophs associated with a phytoplankton bloom in a temperate coastal environment. Appl. Environ. Microbiol. 74: 7321– 7328.

95. Neufeld, J. D.,, M. G. Dumont,, J. Vohra, and, J. C. Murrell. 2007b. Methodological considerations for the use of stable isotope probing in microbial ecology. Microb. Ecol. 53: 435– 442.

96. Neufeld, J. D.,, H. Schafer,, M. J. Cox,, R. Boden,, I. R. McDonald, and, J. C. Murrell. 2007a. Stable-isotope probing implicates Methylophaga spp. and novel Gammaproteobacteria in marine methanol and methylamine metabolism. ISME J. 1: 480– 491.

97. Neufeld, J. D.,, M. Wagner, and, J. C. Murrell. 2007c. Who eats what, where and when? Isotope-labelling experiments are coming of age. ISME J. 1: 103– 110.

98. Noll, M.,, P. Frenzel, and, R. Conrad, 2008. Selective stimulation of type I methanotrophs in a rice paddy soil by urea fertilization revealed by RNA-based stable isotope probing. FEMS Microbiol. Ecol. 65: 125– 132.

99. Oka, A. R.,, C. D. Phelps,, L. M. McGuinness,, A. Mumford,, L. Y. Young, and, L. J. Kerkhof. 2008. Identification of critical members in a sulfidogenic benzene-degrading consortium by DNA stable isotope probing. Appl. Environ. Microbiol. 74: 6476– 6480.

100. Orphan, V. J., and, C. H. House. 2009. Geobological investigations using secondary ion mass spectrometry: Microanalysis of extant and paleo-micorbial processes. Geobiology 7: 360– 372.

101. Orphan, V. J.,, C. H. House,, K. U. Hinrichs,, K. D. McKeegan, and, E. F. DeLong. 2001. Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293: 484– 487.

102. Orphan, V. J.,, C. H. House,, K. U. Hinrichs,, K. D. McKeegan, and, E. F. DeLong. 2002. Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc. Natl. Acad. Sci. USA 99: 7663– 7668.

103. Osaka, T.,, Y. Ebie,, S. Tsuneda, and, Y. Inamori. 2008. Identification of the bacterial community involved in methane-dependent denitrification in activated sludge using DNA stable-isotope probing. FEMS Microbiol. Ecol. 64: 494– 506.

104. Osaka, T.,, S. Yoshie,, S. Tsuneda,, A. Hirata,, N. Iwami, and, Y. Inamori. 2006. Identification of acetate- or methanol-assimilating bacteria under nitrate-reducing conditions by stable-isotope probing. Microb. Ecol. 52: 253– 266.

105. Ouverney, C. C., and, J. A. Fuhrman. 1999. Combined microautoradiography–16s rRNA probe technique for determination of radioisotope uptake by specific microbial cell types in situ. Appl. Environ. Microbiol. 65: 1746– 1752.

106. Padmanabhan, P.,, S. Padmanabhan,, C. DeRito,, A. Gray,, D. Gannon,, J. R. Snape,, C. S. Tsai,, W. Park,, C. Jeon, and, E. L. Madsen. 2003. Respiration of 13C-labeled substrate added to soil in the field and subsequent 16S rRNA gene analysis of 13C-labeled soil DNA. Appl. Environ. Microbiol. 69: 1614– 1622.

107. Pelz, O.,, A. Chatzinotas,, N. Andersen,, S. M. Bernasconi,, C. Hesse,, W.-R. Abraham and, J. Zeyer. 2001. Use of isotopic and molecular techniques to link toluene degradation in denitrifying aquifer microcosms to specific microbial populations. Arch. Microbiol. 175: 270– 281.

108. Pinkart, H. C.,, D. B. Ringelberg,, Y. M. Piceno,, S. J McNaughton, and, D. C. White. 2002. Biochemical approaches to biomass measurements and community structure analysis, p. 91–101. In C. J. Hurst,, R. L. Crawford,, G. R. Knudsen,, M. I. McInerney, and, L. D. Stetzenbach (ed.), Manual of Environmental Microbiology, 2nd ed. ASM Press, Washington, DC.

109. Powell, S. N.,, D. R. Singleton, and, M. D. Aitkin. 2008. Effects of enrichment with salicylate on bacterial selection and PAH mineralization in a microbial community from a bioreactor treating contaminated soil. Environ. Sci. Technol. 42: 4099– 4105.

110. Prosser, J. I.,, J. I. Rangel-Castro, and, K. Killham. 2006. Studying plant-microbe interactions using stable isotope technologies. Curr. Opin. Biotechnol. 17: 98– 102.

111. Pumphrey, G. M.,, B. T. Hanson,, S. Chandra, and, E. L. Madsen. 2009. Dynamic secondary ion mass spectrometry (SIMS) imaging of microbial populations utilizing 13C-labeled substrates in pure culture and in soil. Environ. Microbiol. 11: 220– 229.

112. Pumphrey, G. M., and, E. L. Madsen. 2008. Field-based stable isotope probing reveals the identities of benzoic acid-metabolizing microorganisms and their in situ growth in agricultural soil. Appl. Environ. Microbiol. 74: 4111– 4118.

113. Qiu, Q.,, M. Noll,, W.-R. Abraham,, Y. Lu, and, R. Conrad. 2008. Applying stable isotope probing of phospholipid fatty acids and rRNA in a Chinese rice field to study activity and composition of the methanotrophic bacterial communities in situ. ISME J. 2: 602– 614.

114. Radajewski, S.,, I. R McDonald, and, J. C. Murrell. 2003. Stable-isotope probing of nucleic acids: a window to the function of uncultured microorganisms. Curr. Opin. Biotechnol. 14: 296– 302.

115. Radajewski, S.,, G. Webster,, D. S. Reay,, S. A. Morris,, P. Ineson,, D. B. Nedwell,, J. I. Prosser, and, J. C. Murrell. 2002. Identification of active methylotroph populations in an acidic forest soil by stable-isotope probing. Microbiology 148: 2331– 2342.

116. Radajewski, S.,, P. Ineson,, N. R. Parekh, and, J. C. Murrell. 2000. Stable-isotope probing as a tool in microbial ecology. Nature 403: 646– 649.

117. Roh, H.,, C.-P. Yu,, M. E. Fuller, and, K.-H. Chu. 2009. Identification of Hexahydro-1,3,5-trinitro-1,3,5-triazine-degrading microorganisms via 15N-dtable isotope probing. Environ. Sci. Technol. 43: 2505– 2511.

118. Roslev, P., and, N. Iversen, 1999. Radioactive fingerprinting of microorganisms that oxidize atmospheric methane in different soils. Appl. Environ. Microbiol. 65: 4064– 4070.

119. Saito, T.,, S. Ishii,, S. Otsuka,, M. Nishiyama, and, K. Senoo. 2008. Identification of novel Betaproteobacteria in a succinate-assimilating population in denitrifying rice paddy soil by using stable isotope probing. Microbes Environ. 23: 192– 200.

120. Singh, B. K., and, K. Tate. 2007. Biochemical and molecular characterization of methanotrophs in soil from a pristine New Zealand beech forest. FEMS Microbiol. Lett. 275: 89– 97.

121. Singh, B. K.,, K. R. Tate,, G. Kolipaka,, C. B. Hedley,, C. A. Macdonald,, P. Millard, and, J. C. Murrell. 2007. Effect of afforestation and reforestation of pastures on the activity and population dynamics of methanotrophic bacteria. Appl. Environ. Microbiol. 73: 5153– 5161.

122. Singleton, D. R.,, M. Hunt,, S. N. Powell,, R. Frontera-Suau, and, M. D. Aitken. 2007. Stable-isotope probing with multiple growth substrates to determine substrate specificity of uncultivated bacteria. J. Microbiol. Meth. 69: 180– 187.

123. Singleton, D. R.,, S. N. Powell,, R. Sangaiah,, A. Gold,, L. M. Ball, and, M. D. Aitken. 2005. Stable-isotope probing of bacteria capable of degrading salicylate, naphthalene, or phenanthrene in a bioreactor treating contaminated soil. Appl. Environ. Microbiol. 71: 1202– 1209.

124. Singleton, D. R.,, L. G. Ramirez, and, M. D. Aitken. 2009. Characterization of a polycyclic aromatic hydrocarbon degradation gene cluster in a phenanthrene-degrading Acidovorax strain. Appl. Environ. Microbiol. 75: 2613– 2620.

125. Singleton, D. R.,, R. Sangaiah,, A. Gold,, L. M. Ball, and, M. D. Aitken. 2006. Identification and quantification of uncultivated Proteobacteria associated with pyrene degradation in a bioreactor treating PAH-contaminated soil. Environ. Microbiol. 8: 1736– 1745.

126. Stelzer, N.,, C. Buning,, F. Pfeifer,, A. B. Dohrmann,, C. C. Tebbe,, I. Nijenhuis,, M. Kastner, and, H. H. Richnow. 2006. In situ microcosms to evaluate natural attenuation potentials in contaminated aquifers. Org. Geochem. 37: 1394– 1410.

127. Sueoka, K.,, H. Satoh,, M. Onuki, and, T. Mino. 2009. Microorganisms involved in anaerobic phenol degradation in the treatment of synthetic coke-oven wastewater detected by RNA stable-isotope probing. FEMS Microbiol. Lett. 291: 169– 174.

128. Sul, W. J.,, J. Park,, J. F. Quensen,, J. L. M. Rodrigues,, L. Seliger,, T. V. Tsoi,, G. J. Zylstra, and, J. M. Tiedje. 2009. DNA-stable isotope probing integrated with metagenomics for retrieval of biphenyl dioxygenase genes from polychlorinated biphenyl-contaminated river sediment. Appl. Environ. Microbiol. 75: 5501– 5506.

129. Tanner, M. A.,, B. M. Goebel,, M. A. Dojka, and, N. R. Pace. 1998. Specific ribosomal DNA sequences from diverse environmental settings correlate with experimental contaminants. Appl. Environ. Microbiol. 64: 3110– 3113.

130. Tate, K. R.,, D. J. Ross,, S. Saggar,, C. B. Hedley,, J. Dando,, B. K. Singh, and, S. M. Lambie. 2007. Methane uptake in soils from Pinus radiata plantations, a reverting shrubland and adjacent pastures: effects of land-use change, and soil texture, water and mineral nitrogen. Soil Biol. Biochem. 39: 1437– 1449.

131. Tillmann, S.,, C. Stroempl,, K. N. Timmis, and, W.-R. Abraham. 2005. Stable isotope probing reveals the dominant role of Burkholderia species in aerobic degradation of PCBs. FEMS Microbiol. Ecol. 52: 207– 217.

132. Treude, T.,, V. Orphan,, K. Knittel,, A. Gieseke,, C. H. House, and, A. Boetius. 2007. Consumption of methane and CO 2 by methanotrophic microbial mats from gas seeps of the anoxic Black Sea. Appl. Environ. Microbiol. 73: 2271– 2283.

133. Uhlik, O.,, K. Jecna,, M. B. Leigh,, M. Macková, and, T. Macek. 2009. DNA-based stable isotope probing: a link between community structure and function Sci. Total Environ. 407: 3611– 3619.

134. Uhlik, O.,, K. Jecna,, M. Mackova,, C. Vicek,, M. Hroudova,, K. Demrova,, V. Paces, and, T. Macek. 2009. Biphenyl-metabolizing bacteria in the rhizosphere of horseradish and bulk soil contaminated by polychlorinated biphenyls as revealed by stable isotope probing. Appl. Environ. Microbiol. 75: 6471– 6477.

135. Wagner, M. 2009. Single-cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. Annual Rev. Microbiol. 63: 411– 429.

136. Wagner, M.,, M. Horn, and, H. Daims, 2003. Fluorescence in situ hybridization for the identification and characterisation of prokaryotes. Curr. Opin. Microbiol. 6: 302– 309.

137. Wagner, M., and, A. S. Whitely. 2007. Single cell stable isotope probing with FISH-Raman spectroscopy for deciphering the ecophysiology of uncultured bacteria. FEBS J. 274: 13.

138. Wellington, E. M. H.,, A. Berry, and, M. Krsek. 2003. Resolving functional diversity in relation to microbial community structure in soil: Exploiting genomics and stable isotope probing. Curr. Opin. Biotechnol. 6: 295– 301.

139. Yagi. J. M.,, D. Sims,, T. Brettin,, D. Bruce, and, E. L. Madsen. 2009. Remarkable physiological versatility revealed by whole-genome analysis of the aromatic-hydrocarbon-degrading bacterium, Polaromonas naph-thalenivorans. Environ. Microbiol. 11: 2253– 2270.

140. Yu, C.-P., and, Chu, K.-H. 2005. A quantitative assay for linking microbial community function and structure of a naphthalene-degrading microbial consortium. Environ. Sci. Technol. 39: 9611– 9619.

Tables

Stable Isotope Probing Techniques and Bioremediation

/content/10.1128/9781555816896.ch09.ch09tab01

TABLE 1.

Defining biodegradation and bioremediation

TABLE 1.

Defining biodegradation and bioremediation

/content/10.1128/9781555816896.ch09.ch09tab02

TABLE 2.

Survey of studies using SIP techniques to examine microbial populations responsible for biodegradation of aromatic compounds a

TABLE 2.

Survey of studies using SIP techniques to examine microbial populations responsible for biodegradation of aromatic compounds a

/content/10.1128/9781555816896.ch09.ch09tab03

TABLE 3.

Survey of studies using SIP techniques to examine microbial populations responsible for biodegradation of C1 compoundsa

TABLE 3.

Survey of studies using SIP techniques to examine microbial populations responsible for biodegradation of C1 compoundsa

/content/10.1128/9781555816896.ch09.ch09tab04

TABLE 4.

Survey of studies using SIP techniques to examine microbial populations responsible for biodegradation of organic acids, sugars, and other compounds

TABLE 4.

Survey of studies using SIP techniques to examine microbial populations responsible for biodegradation of organic acids, sugars, and other compounds

/content/10.1128/9781555816896.ch09.ch09tab05

TABLE 5.

Experimental issues confronted by investigators when implementing SIP assays a

TABLE 5.

Experimental issues confronted by investigators when implementing SIP assays a