Protein-based stable isotope probing (Protein-SIP) reveals active species within anoxic mixed cultures

ISME Journal

Volumn 2, Issue 11, 2008, Pages 1122-1133

  Jehmlich, Nico ^a   Schmidt, Frank ^a   Von Bergen, Martin ^a   Richnow, Hans Hermann ^a   Vogt, Carsten ^a  

^a HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

Author keywords

13C7 toluene; Aromatoleum aromaticum strain EbN1; Metabolic labelling; Stable isotope probing (SIP)

Indexed keywords

BACTERIAL PROTEIN; CARBON; GLUCONIC ACID; PROTEOME; TOLUENE;

ANAEROBIC GROWTH; ARTICLE; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; ISOTOPE LABELING; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; RHODOCYCLACEAE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANAEROBIOSIS; BACTERIAL PROTEINS; CARBON; CARBON ISOTOPES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GLUCONATES; ISOTOPE LABELING; MASS SPECTROMETRY; PROTEOME; RHODOCYCLACEAE; TOLUENE;

BACTERIA (MICROORGANISMS);

EID: 55549089274     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2008.64     Document Type: Article

References (54)

1. Barreiros L, Nogales B, Manaia CM, Ferreira ACS, Pieper DH, Reis MA et al. (2003). A novel pathway for mineralization of the thiocarbamate herbicide molinate by a defined bacterial mixed culture. Environ Microbiol 5: 944-953.
2. Benndorf D, Balcke GU, Harms H, von Bergen M. (2007). Functional metaproteome analysis of protein extracts from contaminated soil and groundwater. ISMEJ 1: 224-234.
3. Benndorf D, Müller A, Bock K, Manuwald O, Herbarth O, von Bergen M. (2008). Identification of spore allergens from the indoor mould Aspergillus versicolor. Allergy 63: 454-460.
4. Biegert T, Fuchs G, Heider F. (1996). Evidence that anaerobic oxidation of toluene in the denitrifying bacterium Thauera aromatica is initiated by formation of benzylsuccinate from toluene and fumarate. Eur J Biochem 238: 661-668.
5. Boll M, Albracht SSP, Fuchs G. (1997). Benzoyl-CoA reductase (dearomatizing), a key enzyme of anaerobic aromatic metabolism - A study of adenosinetriphosphatase activity, ATP stoichiometry of the reaction and EPR properties of the enzyme. Eur J Biochem 244: 840-851.
6. Boschker HTS, Nold SC, Wellsbury P, Bos D, de Graaf W, Pel R et al. (1998). Direct linking of microbial populations to specific biogeochemical processes by C-13-labelling of biomarkers. Nature 392: 801-805.
7. Bradford MM. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
8. Bull ID, Parekh NR, Hall GH, Ineson P, Evershed RP. (2000). Detection and classification of atmospheric methane oxidizing bacteria in soil. Nature 405: 175-178.
9. Cargile BJ, Bundy JL, Grunden AM, Stephenson JL. (2004). Synthesis/degradation ratio mass spectrometry for measuring relative dynamic protein turnover. Anal Chem 76: 86-97.
10. Drzyzga O, EL Mamouni R, Agathos SN, Gottschal JC. (2002). Dehalogenation of chlorinated ethenes and immobilization of nickel in anaerobic sediment columns under sulfidogenic conditions. Environ Sci Technol 36: 2630-2635.
11. Dumont MG, Murrell JC. (2005). Stable isotope probing - linking microbial identity to function. Nat Rev Microbiol 3: 499-504.
12. Fischer A, Herklotz I, Herrmann S, Thullner M, Weelink SAB, Stams AJM et al. (2008). Combined carbon and hydrogen isotope fractionation investigations for elucidating benzene biodegradation pathways. Environ Sci Technol; doi:10.1021/es702468f.
13. Friedrich MW. (2006). Stable-isotope probing of DNA: insights into the function of uncultivated microorganisms from isotopically labeled metagenomes. Curr Opin Biotechnol 17: 59-66.
14. Georgieva D, Risch M, Kardas A, Buck F, von Bergen M, Betzel C. (2008). Comparative analysis of the venom proteomes of Vipera ammodytes ammodytes and Vipera ammodytes meridionalis. J Proteome Res 7: 866-886.
15. Geyer R, Peacock AD, Miltner A, Richnow HH, White DC, Sublette KL et al. (2005). In situ assessment of biodegradation potential using biotraps amended with C-13-labeled benzene or toluene. Environ Sci Technol 39: 4983-4989.
16. Hanson JR, Macalady JL, Harris D, Scow KM. (1999). Linking toluene degradation with specific microbial populations in soil. Appl Environ Microbiol 65: 5403-5408.
17. Hehemann JH, Redecke L, Murugaiyan J, von Bergen M, Betzel C, Saborowski R. (2008). Autoproteolytic stability of a trypsin from the marine crab Cancer pagurus. Biochem Biophys Res Commun 370: 566-571.
18. Hugenholtz P, Goebel BM, Pace NR. (1998). Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180: 4765-4774.
19. Hutchens E, Radajewski S, Dumont MG, McDonald IR, Murrell JC. (2004). Analysis of methanotrophic bacteria in Movile Cave by stable isotope probing. Environ Microbiol 6: 111-120.
20. Jimenez L, Breen A, Thomas N, Federle TW, Sayler GS. (1991). Mineralization of linear alkylbenzene sulfonate by a 4-member aerobic bacterial consortium. Appl Environ Microbiol 57: 1566-1569.
21. Johnson KL, Muddiman DC. (2004). A method for calculating O-16/O-18 peptide ion ratios for the relative quantification of proteomes. J Am Soc Mass Spectrom 15: 437-445.
22. Keller M, Zengler K. (2004). Tapping into microbial diversity. Nat Rev Microbiol 2: 141-150.
23. Koch R. (1881). Zur Untersuchung von pathogenen Organismen. Mittheilungen aus dem kaiserlichen Gesundheitsamte 1: 1-48.
24. Krüger M, Wolters H, Gehre M, Richnow HH. (2008). Tracing the slow growth of anaerobic methane oxidising communities by N-15 labelling techniques. Fems Microbiol Ecol 63: 401-411.
25. 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 potentially active populations by stable isotope probing. Environ Microbiol 6: 1049-1060.
26. Lo I, Denef VJ, VerBerkmoes NC, Shah MB, Goltsman D, DiBartolo G et al. (2007). Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446: 537-541.
27. Manefield M, Whiteley AS, Griffiths RI, Bailey MJ. (2002). RNA stable isotope probing, a novel means of linking microbial community function to phylogeny. Appl Environ Microbiol 68: 5367-5373.
28. 2 into different compounds of soil microbial biomass and soil organic matter. Isotopes Environ Health Stud 41: 135-140.
29. Neuhoff V, Arold N, Taube D, Ehrhardt W. (1988). Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9: 255-262.
30. Nijenhuis I, Stelzer N, Kastner M, Richnow HH. (2007). Sensitive detection of anaerobic monochlorobenzene degradation using stable isotope tracers. Environ Sci Technol 41: 3836-3842.
31. Ong SE, Mann M. (2005). Mass spectrometry-based proteomics turns quantitative. Nat Chem Biol 1: 252-262.
32. Pace NR. (1997). A molecular view of microbial diversity and the biosphere. Science 276: 734-740.
33. Pelz O, Chatzinotas A, Andersen N, Bernasconi SM, Hesse C, Abraham WR et al. (2001a). Use of isotopic and molecular techniques to link toluene degradation in denitrifying aquifer microcosms to specific microbial populations. Arch Microbiol 175: 270-281.
34. Pelz O, Chatzinotas A, Zarda-Hess A, Abraham WR, Zeyer J. (2001b). Tracing toluene-assimilating sulfatereducing bacteria using C-13-incorporation in fatty acids and whole-cell hybridization. Fems Microbiol Ecol 38: 123-131.
35. Pelz O, Tesar M, Wittich RM, Moore ER, Timmis KN, Abraham WR. (1999). Towards elucidation of microbial community metabolic pathways: unravelling the network of carbon sharing in a pollutant-degrading consortium by immunocapture and isotopic ratio mass spectrometry. Environ Microbiol 1: 167-174.
36. Pfennig N, Eimhjell Ke, Jensen SL. (1965). A new isolate of Rhodospirillum Fulvum group and its photosynthetic pigments. Archiv Fur Mikrobiologie 51: 258.
37. Rabus R. (2005). Functional genomics of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Appl Microbiol Biotechnol 68: 580-587.
38. Rabus R, Kube M, Heider J, Beck A, Heitmann K, Widdel F et al. (2005). The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch Microbiol 183: 27-36.
39. Rabus R, Widdel F. (1995). Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch Microbiol 163: 96-103.
40. Ram RJ, VerBerkmoes NC, Thelen MP, Tyson GW, Baker BJ, Blake RC et al. (2005). Community proteomics of a natural microbial biofilm. Science 308: 1915-1920.
41. Rappe MS, Giovannoni SJ. (2003). The uncultured microbial majority. Annu Rev Microbiol 57: 369-394.
42. Richnow HH, Vieth A, Kaestner M, Gehre M, Meckenstock RU. (2002). Isotope fractionation of toluene: a perspective to characterise microbial in situ degradation. Scientific World Journal 2: 1227-1234.
43. Santos PM, Roma V, Benndorf D, von Bergen M, Harms H, Sa-Correia I. (2007). Mechanistic insights into the global response to phenol in the phenol-biodegrading strain Pseudomonas sp. M1 revealed. Omics 11: 233-251.
44. Schagger H, Aquila H, von Jagow G. (1988). Coomassie blue sodium dodecyl-sulfate polyacrylamide-gel electrophoresis for direct visualization of polypeptides during electrophoresis. Anal Biochem 173: 201-205.
45. Shevchenko A, Jensen ON, Podtelejnikov AV, Sagliocco F, Wilm M, Vorm O et al. (1996). Linking genome and proteome by mass spectrometry: Large-scale identification of yeast proteins from two dimensional gels. Proc Natl Acad Sci USA 93: 14440-14445.
46. Snijders APL, de Vos MGJ, de Koning B, Wright PC. (2005a). A fast method for quantitative proteomics based on a combination between two-dimensional electrophoresis and N-15-metabolic labelling. Electrophoresis 26: 3191-3199.
47. Snijders APL, de Vos MGJ, Wright PC. (2005b). Novel approach for peptide quantitation and sequencing based on N-15 and C-13 metabolic labeling. J Proteome Res 4: 578-585.
48. Snijders APL, Walther J, Peter S, Kinnman I, de Vos MGJ, van de Werken HJG et al. (2006). Reconstruction of central carbon metabolism in Sulfolobus solfataricus using a two-dimensional gel electrophoresis map, stable isotope labelling and DNA microarray analysis. Proteomics 6: 1518-1529.
49. Webster G, Watt LC, Rinna J, Fry JC, Evershed RP, Parkes RJ et al. (2006). A comparison of stable-isotope probing of DNA and phospholipid fatty acids to study prokaryotic functional diversity in sulfate-reducing marine sediment enrichment slurries. Environ Microbiol 8: 1575-1589.
50. Whiteley AS, Manefield M, Lueders T. (2006). Unlocking the 'microbial black box' using RNA-based stable isotope probing technologies. Curr Opin Biotechnol 17: 67-71.
51. Widdel F, Rabus R. (2001). Anaerobic biodegradation of satured and aromatic hydrocarbons. Curr Opin Biotechnol 12: 259-276.
52. Wilmes P, Bond PL. (2006a). Metaproteomics: studying functional gene expression in microbial ecosystems. Trends Microbiol 14: 92-97.
53. Wilmes P, Bond PL. (2006b). Towards exposure of elusive metabolic mixed-culture processes: the application of metaproteomic analyses to activated sludge. Water Sci Technol 54: 217-226.
54. Zengler K, Richnow HH, Rossello-Mora R, Michaelis W, Widdel F. (1999). Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401: 266-269.