Nutrient amendments in soil DNA stable isotope probing experiments reduce the observed methanotroph diversity

Applied and Environmental Microbiology

Volumn 73, Issue 3, 2007, Pages 798-807

  Cébron, Aurélie ^a,e   Bodrossy, Levente ^b   Stralis Pavese, Nancy ^b   Singer, Andrew C ^c   Thompson, Ian P ^c   Prosser, James I ^d   Murrell, J Colin ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b ARC SEIBERSDORF RESEARCH GMBH   (Austria)

^c CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^d Institute of Marine Sciences School of Biological Sciences   (United Kingdom)

^e Faculté des Sciences et Technologies   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DIVERSITY; DENATURING GRADIENT GEL ELECTROPHORESIS; METHANOTROPH ACTIVITY; MINERAL SALTS;

BACTERIA; DNA; ELECTROPHORESIS; GENES; ISOTOPES; PROBES; RNA; SOILS;

BIODIVERSITY;

CARBON 13; RIBOSOME RNA; RNA 16S; SOIL WATER;

DNA; ENVIRONMENTAL CONDITIONS; ISOTOPIC ANALYSIS; METHANOGENIC BACTERIUM; MICROBIAL ACTIVITY; MICROCOSM; SOIL AMENDMENT; SOIL MICROORGANISM; SOIL WATER; SOIL WATER POTENTIAL; SPECIES DIVERSITY; STABLE ISOTOPE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIODIVERSITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DETERMINATION; GENE; INCUBATION TIME; ISOTOPE LABELING; METHANOTROPHIC BACTERIUM; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT DYNAMICS; PMOA GENE; SOIL ANALYSIS; STABLE ISOTOPE PROBING;

CARBON ISOTOPES; DNA, BACTERIAL; ISOTOPE LABELING; METHANE; METHYLOBACTERIACEAE; METHYLOCYSTACEAE; MOLECULAR PROBE TECHNIQUES; MOLECULAR SEQUENCE DATA; OXYGENASES; RNA, RIBOSOMAL, 16S; SALTS; SEQUENCE ANALYSIS, DNA; SOIL; SOIL MICROBIOLOGY; WATER;

BACTERIA (MICROORGANISMS); METHYLOCOCCACEAE; METHYLOCYSTACEAE;

EID: 33846902311     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01491-06     Document Type: Article

References (69)

1. Auman, A. J., S. Stolyar, A. M. Costello, and M. E. Lidstrom. 2000. Molecular characterization of methanotrophic isolates from freshwater lake sediment. Appl. Environ. Microbiol. 66:5259-5266.
2. Bodelier, P. L., P. Roslev, T. Henckel, and P. Frenzel. 2000. Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots. Nature 403:421-424.
3. Bodrossy, L., N. Stralis-Pavese, J. C. Murrell, S. Radajewski, A. Weilharter, and A. Sessitsch. 2003. Development and validation of a diagnostic microbial microarray for methanotrophs. Environ. Microbiol. 5:566-582.
4. Borodina, E., M. J. Cox, I. R. McDonald, and J. C. Murrell. 2005. Use of DNA-stable isotope probing and functional gene probes to investigate the diversity of methyl chloride-utilizing bacteria in soil. Environ. Microbiol. 7:1318-1328.
5. 13C-labeling of biomarkers. Nature 392:801-805.
6. Bourne, D. G., I. R. McDonald, and J. C. Murrell. 2001. Comparison of pmoA PCR primer sets as tools for investigating methanotroph diversity in three Danish soils. Appl. Environ. Microbiol. 67:3802-3809.
7. Bowman, J. P. 1999. The obligate methanotrophic bacteria: Methylococcus, Methylomonas, and Methylosinus. In M. Dworkin (ed.), The prokaryotes. Springer Verlag, New York, NY. http://link.springer-ny. com.
8. 13C-labeled acetate at the field scale: detection of microbes responsible for reduction of U(VI). Environ. Sci. Technol. 39:9039-9048.
9. Costello, A. M., and M. E. Lidstrom. 1999. Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl. Environ. Microbiol. 65:5066-5074.
10. 13C labeling of bacterial lipids in the characterisation of ambient methane-oxidizing bacteria in soils. Organic Geochem. 36:769-778.
11. Dedysh, S. N., W. Liesack, V. N. Khmelenina, N. E. Suzina, Y. A. Trotsenko, J. D. Semrau, A. M. Bares, N. S. Panikov, and J. M. Tiedje. 2000. Methylocella palustris gen. nov., sp. nov., a new methane-oxidizing acidophilic bacterium from peat bogs, representing a novel subtype of serine-pathway methanotrophs. Int. J. Syst. Evol. Microbiol. 3:955-969.
12. 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.
13. Dumont, C. G., and J. C. Murrell. 2005. Stable isotope probing: linking microbial identity to function. Nat. Rev. Microbiol. 3:499-504.
14. Dunfield, P. F., V. N. Khmelenina, N. E. Suzina, Y. A. Trotsenko, and S. N. Dedysh. 2003. Methylocella silvestris sp. nov., a novel methanotroph isolated from an acidic forest cambisol. Int. J. Syst. Evol. Microbiol. 53:1231-1239.
15. Eller, G., and P. Frenzel. 2001. Changes in activity and community structure of methane-oxidizing bacteria over the growth period of rice. Appl. Environ. Microbiol. 67:2395-2403.
16. Feselstein, J. 1989. PHYLIP-phylogeny inference package (version 3.2). Cladistics 5:164-166.
17. 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.
18. 13C-carrier DNA shortens the incubation time needed to detect benzoate-utilizing denitrifying bacteria by stable-isotope probing. Appl. Environ. Microbiol. 71:5192-5196.
19. 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.
20. 2 pulse-labeling of plants in tandem with stable-isotope probing: methodological considerations for examining microbial function in the rhizosphere. J. Microbiol. Methods 58:119-129.
21. Hanson, R. S., and T. E. Hanson. 1996. Methanotrophic bacteria. Microbiol. Rev. 60:439-471.
22. Henckel, T., U. Jackel, S. Schnell, and R. Conrad. 2000. Molecular analyses of novel methanotrophic communities in forest soil that oxidize atmospheric methane. Appl. Environ. Microbiol. 66:1801-1808.
23. Holmes, A. J., N. J. P. Owens, and J. C. Murrell. 1995. Detection of novel marine methanotrophs using phylogenetic and functional gene probes after methane enrichment. Microbiology 141:1947-1955.
24. Holmes, A. J., P. Roslev, I. R. McDonald, N. Iversen, K. Henriksen, and J. C. Murrell. 1999. Characterization of methanotrophic bacterial populations in soils showing atmospheric methane uptake. Appl. Environ. Microbiol. 65:3312-3318.
25. Horz, H. P., V. Rich, S. Avrahami, and B. J. Bohannan. 2005. Methane-oxidizing bacteria in a California upland grassland soil: diversity and response to simulated global change. Appl. Environ. Microbiol. 71:2642-2652.
26. 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.
27. Jensen, S., L. Øvreås, F. L. Daae, and V. Torsvik. 1998. Diversity in methane enrichments from agricultural soil revealed by DGGE separation of PCR amplified 16S rDNA fragments. FEMS Microbiol. Ecol. 26:17-26.
28. Jeon, C. O., W. Park, P. Padmanabhan, C. DeRito, J. R. Snape, and E. L. Madsen. 2003. Discovery of a bacterium, with distinctive dioxygenase, that is responsible for in situ biodegradation in contaminated sediment. Proc. Natl. Acad. Sci. USA 100:13591-13596.
29. Kemp, P. F. 1995. Can we estimate bacterial growth rates from rRNA content?, p. 279-302. In I. Joint (ed.), Molecular ecology of aquatic microbes. NATO ASI series, vol. G38. Springer-Verlag, Berlin, Germany.
30. Kerkhof, L., and B. Ward. 1993. Comparison of nucleic acid hybridization and fluorometry for measurement of RNA/DNA relationship with growth rate in a marine bacterium. Appl. Environ. Microbiol. 59:1303-1307.
31. Knief, C., A. Lipski, and P. F. Dunfield. 2003. Diversity and activity of methanotrophic bacteria in different upland soils. Appl. Environ. Microbiol. 69:6703-6714.
32. Knief, C., and P. F. Dunfield. 2005. Response and adaptation of different methanotrophic bacteria to low methane mixing ratios. Environ. Microbiol. 7:1307-1317.
33. Knief, C., S. Vanitchung, N. W. Harvey, R. Conrad, P. F. Dunfield, and A. Chidthaisong. 2005. Diversity of methanotrophic bacteria in tropical upland soils under different land uses. Appl. Environ. Microbiol. 71:3826-3831.
34. Lane, D. J. 1991. 16S/23S rRNA sequencing, p. 115-175. In M. Goodfellow and E. Stackebrandt (ed.), Nucleic acid techniques in bacterial systematics. John Wiley & Sons, Inc., New York, NY.
35. Lieberman, R. L., and A. C. Rosenzweig. 2004. Biological methane oxidation: regulation, biochemistry, and active site structure of particulate methane monooxygenase. Crit. Rev. Biochem. Mol. Biol. 39:147-164.
36. 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.
37. Lueders, T., B. Wagner, P. Claus, and M. W. Friedrich. 2004. 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.
38. Madsen, E. L. 2006. The use of stable isotope probing techniques in bioreactor and field studies on bioremediation. Curr. Opin. Biotechnol. 17:92-97.
39. 13C-labeled plant materials and ergosterool, PLFA, and NLFA analyses to investigate organic matter decomposition in Antarctic soil. Soil Biol. Biochem. 36:165-175.
40. Manefield, M., A. S. Whiteley, N. Ostle, P. Ineson, and M. J. Bailey. 2002. Technical considerations for RNA-based stable isotope probing: an approach to associating microbial diversity with microbial community function. Rapid Commun. Mass Spectrom. 16:2179-2183.
41. 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.
42. Manefield, M., A. S. Whiteley, and M. J. Bailey. 2004. What can stable isotope probing do for bioremediation? Int. Biodeterior. Biodegrad. 54:163-166.
43. 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 bromine 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.
44. 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.
45. Murrell, J. C., and H. Dalton. 1983. Nitrogen fixation in obligate methanotrophs. J. Gen. Microbiol. 129:3481-3486.
46. Muyzer, G., T. Brinkhoff, U. Nübel, C. Santegoeds, H. Schäfer, and C. Wawer. 1998. Denaturing gradient gel electrophoresis (DGGE) in microbial ecology, p. 1-27. In A. D. L. Akkermans, J. D. van Elsas, and F. J. de Bruijn (ed.), Molecular microbial ecology manual, vol. 3.4.4. Kluwer Academic Publishers, Dordrecht, The Netherlands.
47. Nercessian, O., N. Bienvenu, D. Moreira, D. Prieur, and C. Jeanthon. 2005. Diversity of functional genes of methanogens, methanotrophs and sulfate reducers in deep-sea hydrothermal environments. Environ. Microbiol. 7:118-132.
48. 13C-methane incorporation into methanotroph membrane lipids in freshwater sediment. FEMS Microbiol. Ecol. 29:81-89.
49. 2 spike. Soil Biol. Biochem. 35:877-888.
50. 13C-labeled soil DNA. Appl. Environ. Microbiol. 69:1614-1622.
51. Page, R. D. M. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
52. Pombo, S. A., J. Kleikemper, M. H. Schroth, and J. Zeyer. 2005. Field-scale isotopic labeling of phospholipid fatty acids from acetate-degrading sulfate-reducing bacteria. FEMS Microbiol. Ecol. 51:197-207.
53. 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.
54. 4. Methods Mol. Biol. 179:149-157.
55. Radajewski, S., G. Webster, D. S. Reay, S. A. Morris, P. Ineson, D. B., Nedwell, J. L. Prosser, and J. C. Murrell. 2002. Identification of active methylotroph populations in an acidic forest soil by stable-isotope probing. Microbiology 148:2331-2342.
56. 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.
57. Reay, D. S., S. Radajewski, J. C. Murrell, N. P. McNamara, and D. B. Nedwell. 2001. Impact of land-use on the activity and diversity of methane oxidizing bacteria in forest soils. Soil Biol. Biochem. 33:1613-1623.
58. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
59. Saunders, S. E., and J. F. Burke. 1990. Rapid isolation of miniprep DNA for double strand sequencing. Nucleic Acids Res. 18:4948.
60. 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.
61. Smith, K. S., A. M. Costello, and M. E. Lidstrom. 1997. Methane and trichloroethylene oxidation by an estuarine methanotroph, Methylobacter sp. strain BB5.1. Appl. Environ. Microbiol. 63:4617-4620.
62. Stralis-Pavese, N., A. Sessitsch, A. Weilharter, T. Reichenauer, J. Riesing, J. Csontos, J. C. Murrell, and L. Bodossy. 2004. Optimisation of diagnostic microarray for application in analysing landfill methanotroph communities under different plant covers. Environ. Microbiol. 6:347-363.
63. Tillmann, S., C. Strömpl, 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.
64. Treonis, A. M., N. J. Ostle, A. W. Stott, R. Primrose, S. J. Grayston, and P. Ineson. 2004. Identification of groups of metabolically active rhizosphere microorganisms by stable-isotope probing of PLFAs. Soil Biol. Biochem. 36:533-537.
65. Whitby, C., M. J. Bailey, K. Killham, J. C. Murrell, J. I. Prosser, A. Whiteley, and H. M. Lappin-Scott. 2005. Stable isotope probing links taxonomy with function in microbial communities. ASM News 71:169-173.
66. Whittenbury, R., K. C. Phillips, and J. F. Wilkinson. 1970. Enrichment, isolation and some properties of methane-utilizing bacteria. J. Gen. Microbiol. 61:205-218.
67. Wise, M. G., J. V. McArthur, and L. J. Shimkets. 1999. Methanotroph diversity in landfill soil: isolation of novel type I and type II methanotrophs whose presence was suggested by culture-independent 16S ribosomal DNA analysis. Appl. Environ. Microbiol. 65:4887-4897.
68. Yeates, C., and M. R. Gillings. 1998. Rapid purification of DNA from soil for molecular biodiversity analysis. Lett. Appl. Microbiol. 27:49-53.
69. Yu, C. P., and K. H. Chu. 2005. A quantitative assay for linking microbial community function and structure of a naphthalene-degrading microbial consortium. Environ. Sci. Technol. 39:9611-9619.