Comparison of rRNA and polar-lipid-derived fatty acid biomarkers for assessment of13C-substrate incorporation by microorganisms in marine sediments

Applied and Environmental Microbiology

Volumn 72, Issue 8, 2006, Pages 5246-5253

  MacGregor, Barbara J ^a,c   Boschker, Henricus T S ^b   Amann, Rudolf ^a  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIA; BIOMARKERS; FATTY ACIDS; GLUCOSE; LIPIDS; MARINE BIOLOGY; MICROBIOLOGY; MICROORGANISMS;

ELEMENTAL ANALYSIS-ISOTOPE RATIO MASS SPECTROMETRY; INCUBATION; PARAMAGNETIC BEADS; POLAR-LIPID-DERIVED FATTY ACID (PLFA);

RNA;

ACETIC ACID; AMINO ACID; BIOTIN; CARBON 13; FATTY ACID; GLUCOSE; LIPID; PROPIONIC ACID; RIBOSOME RNA; RNA; SMALL SUBUNIT RIBOSOMAL RNA; STREPTAVIDIN;

BACTERIUM; BIOMARKER; CARBON ISOTOPE; COMMUNITY STRUCTURE; EUKARYOTE; FATTY ACID; ISOTOPIC ANALYSIS; MARINE SEDIMENT; RNA;

ARTICLE; ATLANTIC OCEAN; BACTERIAL GROWTH; COMMUNITY STRUCTURE; COMPARATIVE STUDY; CONTROLLED STUDY; ECOSYSTEM; EUKARYOTE; ISOTOPE LABELING; MASS SPECTROMETRY; MICROBIAL POPULATION DYNAMICS; NONHUMAN; OLIGONUCLEOTIDE PROBE; RIBOSOME; RNA ISOLATION; RNA SEQUENCE; SEDIMENT; SENSITIVITY AND SPECIFICITY;

ANIMALS; BACTERIA; BIOLOGICAL MARKERS; BIVALVIA; CARBON ISOTOPES; EUKARYOTIC CELLS; FATTY ACIDS; GEOLOGIC SEDIMENTS; GILLS; LIPIDS; RNA, RIBOSOMAL;

ATLANTIC OCEAN; NORTH SEA;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 33747346478     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00423-06     Document Type: Article

References (65)

1. Acimovic, Y., and I. R. Coe. 2002. Molecular evolution of the equilibrative nucleoside transporter family: identification of novel family members in prokaryotes and eukaryotes. Mol. Biol. Evol. 19:2199-2210.
2. Alm, E. W., D. B. Oerther, N. Larsen, D. A. Stahl, and L. Raskin. 1996. The oligonucleotide probe database. Appl. Environ. Microbiol. 62:3557-3559.
3. Alm, E. W., and D. A. Stahl. 2000. Critical factors influencing the recovery and integrity of rRNA extracted from environmental samples: use of an optimized protocol to measure depth-related biomass distribution in freshwater sediments. J. Microbiol. Methods 40:153-162.
4. Amann, R. I., B. J. Binder, R. J. Olson, S. W. Chisholm, R. Devereux, and D. A. Stahl. 1990. Combination of 16S ribosomal RNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56:1919-1925.
5. Baker, B. J., P. Hugenholtz, S. C. Dawson, and J. F. Banfield. 2003. Extremely acidophilic protists from acid mine drainage host Rickettsiales- lineage endosymbionts that have intervening sequences in their 16S rRNA genes. Appl. Environ. Microbiol. 69:5512-5518.
6. Bergin, C. 2002. Charakterisierung von stabilen Kohlenstoffisotopen in Gewehe und RNA von Muscheln mit endosymbiontischen Bakterien. Diplomarbeit. Ernst-Moritz-Arndt-Universität, Greifswald, Germany.
7. Bergin, C., P. R. Dando, N. Dubilier, and B. J. MacGregor. 2003. Stable carbon isotopic composition of RNA and SSU rRNA in the hydrothermal vent mussel Bathymodiolus azoricus harboring a dual endosymbiont population. Presented at the ASLO Aquatic Sciences Meeting, Salt Lake City, Utah.
8. Beste, D. J. V., J. Peters, T. Hooper, C. Avignone-Rossa, M. E. Bushell, and J. McFadden. 2005. Compiling a molecular inventory for Mycobacterium bovis BCG at two growth rates: evidence for growth rate-mediated regulation of ribosome biosynthesis and lipid metabolism. J. Bacteriol. 187:1677-1684.
9. Biagini, G. A., A. J. Rutter, B. J. Finlay, and D. Lloyd. 1998. Lipids and lipid metabolism in the microaerobic free-living diplomonad Hexamita sp. Eur. J. Protistol. 34:148-152.
10. 13C) labeling in combination with PLFA analysis, p. 1673-1688. In G. A. Kowalchuk, F. J. de Bruijn, I. M. Head, A. D. Akkermans, and J. D. van Elsas (ed.), Microbial ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands.
11. 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.
12. Boschker, H. T. S., and J. J. Middelburg. 2002. Stable isotopes and biomarkers in microbial ecology. FEMS Microbiol. Ecol. 40:85-95.
13. 13C-labelling of biomarkers. Nature 392:801-805.
14. Bowman, J. P., and R. D. McCuaig. 2003. Biodiversity, community structural shifts, and biogeography of prokaryotes within Antarctic continental shelf sediment. Appl. Environ. Microbiol. 69:2463-2483.
15. Brinch-Iversen, J., and G. M. King. 1990. Effects of substrate concentration, growth state, and oxygen availability on relationships among bacterial carbon, nitrogen and phospholipid phosphorus content. FEMS Microbiol. Ecol. 74:345-355.
16. Buchan, A., S. Y. Newell, M. Butler, E. J. Biers, J. T. Hollibaugh, and M. A. Moran. 2003. Dynamics of bacterial and fungal communities on decaying salt marsh grass. Appl. Environ. Microbiol. 69:6676-6687.
17. 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.
18. Canfield, D. E., E. Kristensen, and B. Thamdrup. 2005. Aquatic geomicrobiology, vol. 48. Advances in Marine Biology. Elsevier, Oxford, United Kingdom.
19. Cox, R. A. 2004. Quantitative relationships for specific growth rates and macromolecular compositions of Mycobacterium tuberculosis, Streptomyces coelicolor A3(2) and Escherichia coli B/r: an integrative theoretical approach. Microbiology 150:1413-1426.
20. Daims, H., A. Bruhl, R. Amann, K. H. Schleifer, and M. Wagner. 1999. The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst. Appl. Microbiol. 22:434-444.
21. de Koning, H., and G. Diallinas. 2000. Nucleobase transporters (review). Mol. Membr. Biol. 17:75-94.
22. Dell'Anno, A., M. Fabiano, G. C. A. Duineveld, A. Kok, and R. Danovaro. 1998. Nucleic acid (DNA, RNA) quantification and RNA/DNA ratio determination in marine sediments: comparison of spectrophotometric, fluorometric, and high-performance liquid chromatography methods and estimation of detrital DNA. Appl. Environ. Microbiol. 64:3238-3245.
23. de Vries, J., and W. Wackernagel. 2004. Microbial horizontal gene transfer and the DNA release from transgenic crop plants. Plant Soil 266:91-104.
24. Dubnau, D. 1999. DNA uptake in bacteria. Annu. Rev. Microbiol. 53:217-244.
25. Fang, J. S., C. Kato, T. Sato, O. Chan, and D. McKay. 2004. Biosynthesis and dietary uptake of polyunsaturated fatty acids by piezophilic bacteria. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 137:455-461.
26. Fegatella, F., J. Lim, S. Kjelleberg, and R. Cavicchioli. 1998. Implications of rRNA operon copy number and ribosome content in the marine oligotrophic ultramicrobacterium Sphingomonas sp. strain RB2256. Appl. Environ. Microbiol. 64:4433-4438.
27. Flärdh, K., P. S. Cohen, and S. Kjelleberg. 1992. Ribosomes exist in large excess over the apparent demand for protein synthesis during carbon starvation in marine Vibrio sp. strain CCUG 15956. J. Bacteriol. 174:6780-6788.
28. Freitag, T. E., and J. I. Prosser. 2003. Community structure of ammonia-oxidizing bacteria within anoxic marine sediments. Appl. Environ. Microbiol. 69:1359-1371.
29. Fuchs, B. M., F. O. Glöckner, J. Wülf, and R. Amann. 2000. Unlabeled helper oligonucleotides increase the in situ accessibility to 16S rRNA of fluorescently labeled oligonucleotide probes. Appl. Environ. Microbiol. 66:3603-3607.
30. 13C-carrier DNA shortens the incubation time needed to detect benzoate-utilizing denitrifying bacteria by stable-isotope probing. Appl. Environ. Microbiol. 71:5192-5196.
31. Godin, J.-P., J. Hau, L.-B. Fay, and G. Hopfgartner. 2005. Isotope ratio monitoring of small molecules and macromolecules by liquid chromatography coupled to isotope ratio mass spectrometry. Rapid Commun. Mass Spectrom. 19:2689-2698.
32. Hanson, J. R., J. L. Macalady, D. Harris, and K. M. Scow. 1999. Linking toluene degradation with specific microbial populations in soil. Appl. Environ. Microbiol. 65:5403-5408.
33. Head, I. M., J. R. Saunders, and R. W. Pickup. 1998. Microbial evolution, diversity, and ecology: a decade of ribosomal RNA analysis of uncultivated microorganisms. Microb. Ecol. 35:1-21.
34. Hicks, R. E., R. I. Amann, and D. A. Stahl. 1992. Dual staining of natural bacterioplankton with 4′,6-diamidino-2-phenylindole and fluorescent oligonucleotide probes targeting kingdom-level 16S ribosomal RNA sequences. Appl. Environ. Microbiol. 58:2158-2163.
35. Jørgensen, B. B. 1978. Comparison of methods for the quantification of bacterial sulfate reduction in coastal marine sediments. I. Measurement with radiotracer techniques. Geomicrobiol. J. 1:11-27.
36. Ju, Q. D., and J. R. Warner. 1994. Ribosome synthesis during the growth cycle of Saccharomyces cerevisiae. Yeast 10:151-157.
37. Kemp, P. F., and J. Y. Aller. 2004. Bacterial diversity in aquatic and other environments: what 16S rDNA libraries can tell us. FEMS Microbiol. Ecol. 47:161-177.
38. Kerkhof, L., and P. Kemp. 1999. Small ribosomal RNA content in marine proteobacteria during non-steady-state growth. FEMS Microbiol. Ecol. 30:253-260.
39. Krummen, M., A. W. Hilkert, D. Juchelka, A. Duhr, H. J. Schlüter, and R. Pesch. 2004. A new concept for isotope ratio monitoring liquid chromatography/mass spectrometry. Rapid Commun. Mass Spectrom. 18:2260-2266.
40. Lim, E. L., L. A. Amaral, D. A. Caron, and E. F. DeLong. 1993. Application of ribosomal RNA-based probes for observing marine nanoplanktonic prolists. Appl. Environ. Microbiol. 59:1647-1655.
41. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Förster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. König, T. Liss, R. Lüßmann, M. May, B. Nonhoff, B. Reichel, R. Strehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, and K.-H. Schleifer. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
42. Lueders, T., M. Manefield, and M. W. Friedrich. 2004. Enhanced sensitivity of DNA- and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environ. Microbiol. 6:73-78.
43. Lyons, J. I., S. Y. Newell, R. P. Brown, and M. A. Moran. 2005. Screening for bacterial-fungal associations in a south-eastern US salt marsh using pre-established fungal monocultures. FEMS Microbiol. Ecol. 54:179-187.
44. MacGregor, B. J., V. Brüchert, S. Fleischer, and R. Amann. 2002. Isolation of small-subunit rRNA for stable isotopic characterization. Environ. Microbiol. 4:451-464.
45. MacGregor, B. J., and D. Juchelka. 2005. Determining stable carbon isotopic composition of rRNA by HPLC-IRMS: a new method to discover who is eating what in microbial communities. Presented at the ASLO Aquatic Sciences Meeting, Salt Lake City, Utah.
46. MacGregor, B. J., D. P. Moser, E. W. Alm, K. H. Nealson, and D. A. Stahl. 1997. Crenarchaeota in Lake Michigan sediment. Appl. Environ. Microbiol. 63:1178-1181.
47. 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.
48. 13C-labeling study. Limnol. Oceanog. 45:1224-1234.
49. Mulder, M. M., H. M. L. van der Gulden, P. W. Postma, and K. van Dam. 1988. Effect of macromolecular composition of microorganisms on the thermodynamic description of their growth. Biochim. Biophys. Acta 936:406-412.
50. Neidhardt, F. C., and H. E. Umbarger. 2004, posting date. Chemical composition of E. coli. In Escherichia coli and Salmonella: cellular and molecular biology. American Society for Microbiology, Washington, D.C. [Online.] http://www.ecosal.org/ecosal/index.jsp.
51. Nelson, D. L., and M. M. Cox. 2004. Lehninger principles of biochemistry. W. H. Freeman, New York, N.Y.
52. Pearson, A., A. L. Sessions, K. J. Edwards, and J. M. Hayes. 2004. Phylogenetically specific separation of rRNA from prokaryotes for isotopic analysis. Mar. Chem. 92:295-306.
53. Pelz, O., M. Tesar, R. M. Wittich, E. R. B. Moore, K. N. Timmis, and W. R. Abraham. 1999. Towards elucidation of microbial community metabolic pathways: unraveling the network of carbon sharing in a pollutant-degrading bacterial consortium by immunocapture and isotopic ratio mass spectrometry. Environ. Microbiol. 1:167-174.
54. Pernthaler, A., J. Pernthaler, H. Eilers, and R. Amann. 2001. Growth patterns of two marine isolates: adaptations to substrate patchiness? Appl. Environ. Microbiol. 67:4077-4083.
55. 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.
56. Ravenschlag, K., K. Sahm, and R. Amann. 2001. Quantitative molecular analysis of the microbial community in marine Arctic sediments (Svalbard). Appl. Environ. Microbiol. 67:387-395.
57. Ravenschlag, K., K. Sahm, J. Pernthaler, and R. Amann. 1999. High bacterial diversity in permanently cold marine sediments. Appl. Environ. Microbiol. 65:3982-3989.
58. Rosset, R., J. Julien, and R. Monier. 1966. Ribonucleic acid composition of bacteria as a function of growth rate. J. Mol. Biol. 18:308-320.
59. Schaechter, M., O. Maaløe, and N. O. Kjeldgaard. 1958. Dependency on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. J. Gen. Microbiol. 19:592-606.
60. Sessions, A. L., S. P. Sylva, and J. M. Hayes. 2005. Moving-wire device for carbon isotopic analyses of nanogram quantities of nonvolatile organic carbon. Anal. Chem. 77:6519-6527.
61. Stahl, D. A., B. Flesher, H. R. Mansfield, and L. Montgomery. 1988. Use of phylogenetically based hybridization probes for studies of ruminal microbial ecology. Appl. Environ. Microbiol. 54:1079-1084.
62. Stoeck, T., and S. Epstein. 2003. Novel eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen-depleted marine environments. Appl. Environ. Microbiol. 69:2657-2663.
63. Tunlid, A., and D. C. White. 1992. Biochemical analysis of biomass, community structure, nutritional status, and metabolic activity of microbial communities in soil, p. 229-262. In J. M. Bollag and G. Stotzky (ed.), Soil biochemistry. Marcel Dekker, New York, N.Y.
64. Vrede, T., D. R. Dobberfuhl, S. A. L. M. Kooijman, and J. J. Elser. 2004. Fundamental connections among organism C:N:P stoichiometry, macromolecular composition, and growth. Ecology 85:1217-1229.
65. Watanabe, K., C. Ishikawa, H. Inoue, D. Cenhua, K. Yazawa, and K. Kondo. 1994. Incorporation of exogenous docosahexaenoic acid into various bacterial lipids. J. Am. Oil Chem. Soc. 71:325-330.