Carbon isotope signatures of fatty acids in Geobacter metallireducens and Shewanella algae

Chemical Geology

Volumn 195, Issue 1-4, 2003, Pages 17-28

  Zhang, Chuanlun L ^a   Li, Yiliang ^a   Ye, Qi ^a   Fong, Jon ^b   Peacock, Aaron D ^c   Blunt, Elizabeth ^d   Fang, Jiasong ^e   Lovley, Derek R ^d   White, David C ^c  

^a UNIVERSITY OF MISSOURI   (United States)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF TENNESSEE   (United States)

^d UNIVERSITY OF MASSACHUSETTS   (United States)

^e The Department of Civil and Environmental Engineering   (United States)

Author keywords

Carbon isotopes; Geobacter metallireducens; Iron reducing bacteria; Lipid biomarkers; Shewanella algae

Indexed keywords

CARBON ISOTOPE; FATTY ACID; IRON-REDUCING BACTERIUM; ISOTOPIC FRACTIONATION; LIPID; MICROBIAL COMMUNITY;

EID: 0037446442     PISSN: 00092541     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0009-2541(02)00386-8     Document Type: Article

References (68)

1. Abraham, W.-R., Hesse, C., Pelz, O., 1998. Ratios of carbon isotopes in microbial lipids as an indicator of substrate usage. Appl. Environ. Microbiol. 64, 4202-4209.
2. 12C ratios in individual fatty acids of marine mytilids with and without bacterial symbionts. Org. Geochem. 21, 611-617.
3. Anthony, C., 1982. The Biochemistry of Methylotrophs. Academic Press, London.
4. Baird, B.H., Nivens, D.E., Parker, J.G., White, D.C., 1985. The biomass, community structure, and spatial distribution of the sedimentary microbiota from a high-energy area of the deep sea. Deep-Sea Res. 32, 1089-1099.
5. Blair, N., Leu, A., Nunoz, E., Olsen, J., Kwong, E., Des Marais, D., 1985. Carbon isotopic fractionation in heterotrophic microbial metabolism. Appl. Environ. Microbiol. 50, 996-1001.
6. Brettar, I., Hoefle, M.G., 1993. Nitrous oxide producing heterotrophic bacteria from the water column of the central Baltic: abundance and molecular identification. Mar. Ecol., Prog. Ser. 94, 253-265.
7. Caccavo Jr., F., Blakemore, R.P., Lovley, D.R., 1992. A hydrogen-oxidizing, Fe(III)-reducing microorganism from the Great Bay Estuary, New Hampshire. Appl. Environ. Microbiol. 58, 3211-3216.
8. Caccavo Jr., F., Lonergan, D.J., Lovley, D.R., Davis, M., Stolz, J.F., McInerney, M.J., 1994. Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl. Environ. Microbiol. 60, 3752-3759.
9. Champine, J.E., Goodwin, S., 1991. Acetate catabolism in the dissimilatory iron-reducing isolate GS-15. J. Bacteriol. 173, 2704-2706.
10. Coates, J.D., Phillips, E.J.P., Lonergan, D.J., Jenter, H., Lovley, D.R., 1996. Isolation of Geobacter species from diverse sedimentary environments. Appl. Environ. Microbiol. 62, 1531-1536.
11. DeNiro, M.J., Epstein, S., 1977. Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197, 261-263.
12. Dowling, N.J.E., Widdel, F., White, D.C., 1986. Phospholipid ester-linked fatty acid biomarkers of acetate-oxidizing sulphate-reducers and other sulphide-forming bacteria. J. Gen. Microbiol. 132, 1815-1825.
13. Fang, J., Abrajano, T.A., Comet, P.A., Brooks, J.M., Sassen, R., MacDonald, I.R., 1993. Gulf of Mexico hydrocarbon seep communities: XI. Carbon isotopic fractionation during fatty acid biosynthesis of seep organisms and its implication for chemosynthetic processes. Chem. Geol. 109, 271-279.
14. Fredrickson, J.K., Gorby, Y.A., 1996. Environmental processes mediated by iron-reducing bacteria. Curr. Opin. Biotechnol. 7, 287-294.
15. Gorby, Y.A., Lovley, D.R., 1992. Enzymatic uranium precipitation. Environ. Sci. Technol. 26, 205-207.
16. Guckert, J.B., Antworth, C.B., Nichols, P.D., White, D.C., 1985. Phospholipid ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol. Ecol. 31, 147-158.
17. 13C contents of sedimentary organic compounds: principles and evidence. Mar. Geol. 113, 111-125.
18. Hayes, J.M., 2001. Fractionation of carbon and hydrogen isotopesin biosynthetic processes. In: Ribbe, P.H. (Ed.), Reviews in Mineralogy and Geochemistry. In: Valley, J.M., Cole, D.R. (Eds.), Stable Isotope Geochemistry, vol. 43. The Mineralogical Society of America, Washington, DC, pp. 225-277.
19. Hayes, J.M., Freeman, K.H., Popp, B.N., Hoham, C.H., 1990. Compound-specific isotopic analyses: a novel tool for reconstruction of ancient biogeochemical processes. Org. Geochem. 16, 1115-1128.
20. Hinrichs, K.-U., Hayes, J.M., Sylva, S.P., Brewer, P.G., DeLong, E.F., 1999. Methane-consuming archaebacteria in marine sediments. Nature 398, 802-805.
21. Hinrichs, K.-U., Sylva, S.P., Hayes, J.M., Summons, R.E., Orphan, V., 2000. Molecular and isotopic analysis of anaerobic methaneoxidizing communities in marine sediments. Org. Geochem. 31, 1685-1701.
22. Jahnke, L.L., Summons, R.E., Hope, J.M., Des Marais, D.J., 1999. Carbon isotopic fractionation in lipids from methanotrophic bacteria: II. The effects of physiology and environmental parameters on the biosynthesis and isotopic signatures of biomarkers. Geochim. Cosmochim. Acta 63, 79-93.
23. Lonergan, D.J., Jenter, H.L., Coates, J.D., Phillips, E.J., Schmidt, T.M., Lovley, D.R., 1996. Phylogenetic analysis of dissimilatory Fe(III)-reducing bacteria. J. Bacteriol. 178, 2402-2408.
24. Lovley, D.R. 1991. Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol. Rev. 55, 259-287.
25. Lovley, D.R., 1995. Bioremediation of organic and metal contaminants with dissimilatory metal reduction. J. Ind. Microbiol. 14, 85-93.
26. lLovley, D.R., 2000. Determination of the structure of metal- and humics-reducing microbial communities in subsurface environments contaminated with uranium and other metals. Abstract for DOE-NABIR Workshop, Department of Energy, Washington DC, Reston, VA.
27. Lovley, D.R., Phillips, E.J., 1988. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 54, 1472-1480.
28. Lovley, D.R., Phillips, E.J.P., Gorby, Y.A., Landa, E.R., 1991. Microbial reduction of uranium. Nature 350, 413-416.
29. Lovley, D.R., Giovannoni, S.J., White, D.C., Champine, J.E., Phillips, E.J.P., Gorby, Y.A., Goodwin, S., 1993. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch. Microbiol. 159, 336-344.
30. Macko, S.A., Engel, M.H., Qian, Y., 1994. Early diagenesis and organic matter preservation - a molecular stable carbon isotope perspective. Chem. Geol. 114, 365-379.
31. Madigan, M.T., Martinko, J.M., Parker, J., 2000. Brock Biology of Microorganisms. 9th ed. Prentice-Hall, Upper Saddle River, NJ.
32. Mariotti, A., Germon, J.C., Hubert, P., Kaiser, P., Letolle, R., Tardieux, A., Tardieux, P., 1981. Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant Soil 62, 413-430.
33. Melzer, E., Schmidt, H.-L., 1987. Carbon isotope effects on the pyruvate dehydrogenase reaction and their importance for relative carbon-13 depletion in lipids. J. Biol. Chem. 262, 8159-8164.
34. Merritt, D.A, Brand, W.A., Hayes, J.M., 1994. Isotope-ratio-monitoring gas chromatography-mass spectrometry: methods for isotopic calibration. Org. Geochem. 21, 573-583.
35. Monson, K.D., Hayes, J.M., 1980. Biosynthetic control of the natural abundance of carbon 13 at specific positions within fatty acids in Escherichia coli. J. Biol. Chem.255, 11435-11441.
36. Monson, K.D., Hayes, J.M., 1982. Carbon isotopic fractionation in the biosynthesis of bacterial fatty acids. Ozonolysis of unsaturated fatty acids as a means of determining the intramolecular distribution of carbon isotopes. Geochim. Cosmochim. Acta 46, 139-149.
37. Moule, A.L., Wilkinson, S.G., 1987. Polar lipids, fatty acids, and isoprenoid quinones of Alteromonas putrefaciens (Shewanella putrefaciens . Syst. Appl. Microbiol. 9, 192-198.
38. Myers, C.R., Nealson, K.H., 1988. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240, 1319-1321.
39. Nealson, K.H., Saffarini, D., 1994. Iron and manganese in anaerobic respiration: Environmental significance, physiology, and regulation. Annu. Rev. Microbiol. 48, 311-343.
40. Nealson, K.H., Myers, C.R., Wimpee, B.B., 1991. Isolation and identification of manganese-reducing bacteria and estimates of microbial Mn(IV)-reducing potential in the Black Sea. Deep-Sea Res. 38, 907-920.
41. Nichols, P.D., Guckert, J.B., White, D.C., 1986. Determination of monounsaturated fatty acid double-bond position and geometry for microbial monocultures and complex microbial consortia by capillary GC/MS of their dimethyl disulfide adducts. J. Microbiol. Methods 5, 49-55.
42. Nichols, D.S., Nichols, P.D., McMeekin, T.A., 1992. Anaerobic production of polyunsaturated fatty acids by Shewanella putrefaciens strain ACAM 342. FEMS Microbiol. Lett. 98, 117-122.
43. Pancost, R.D., Sinninghe Damsté, J.S., 2003. Carbon isotopic compositions of prokaryotic lipids as tracers of carbon cycling in diverse settings. Chem. Geol. (in press).
44. Pancost, R.D., Sinninghe Damsté, J.S., De Lint, S., Van Der Maarel, M.J.E.C., Gottschal, J.C., the Medinaut Shipboard Scientific Party, 2000. Biomarker evidence for widespread anaerobic methane oxidation in Mediterranean sediments by a consortium of methanogenic archaea and bacteria. Appl. Environ. Microbiol. 66, 1126-1132.
45. Pancost, R.D., Hopmans, E.C., Sinninghe Damsté, J.S., the Medinaut Shipboard Scientific Party, 2001. Archaeal lipids in Mediterranean Cold Seeps: molecular proxies for anaerobic methane oxidation. Geochim. Cosmochim. Acta 65, 1611-1627.
46. 2 fixation pathways. J. Biosci. 44C, 397-402.
47. Ricci, M.P., Merritt, D.A., Freeman, K.H., Hayes, J.M., 1994. Acquisition and processing of data for isotope-ratio-monitoring mass spectrometry. Org. Geochem. 21, 561-571.
48. Ringo, E., Stenberg, E., Strom, A.R., 1984. Amino acid and lactate catabolism in trimethylamine oxide respiration of Alteromonas putrefaciens NCMB 1735. Appl. Environ. Microbiol. 47, 1084-1089.
49. Rossello-Mora, R.A., Caccavo Jr., F., Osterlehner, K., Springer, N., Spring, S., Schuler, D., Lugwig, W., Amann, R., Vanncanneyt, M., Schleifer, K.H., 1994. Isolation and taxonomic characterization of a halotolerant, facultatively iron-reducing bacterium. Syst. Appl. Microbiol. 17, 569-573.
50. Sakata, S., Hayes, J.M., McTaggart, A.R., Evans, R.A., Leckrone, K.J., Togasaki, R.K., 1997. Carbon isotopic fractionation associated with lipid biosynthesis by a cyanobacterium: relevance for interpretation of biomarker records. Geochim. Cosmochim. Acta 61, 5379-5389.
51. Schouten, S., Breteler, W.C.M.K., Blokker, P., Schogt, N., Rijpstra, W.I.C., Grice, K., Bass, M., Sinninghe Damsté, J.S., 1998. Biosynthetic effects on the stable carbon isotopic compositions of algal lipids: implications for deciphering the carbon isotopic biomarker record. Geochim. Cosmochim. Acta 62, 1397-1406.
52. Scott, J.H., Nealson, K.H., 1994. A biochemical study of the intermediary carbon metabolism of Shewanella putrefaciens. J. Bacteriol. 176, 3408-3411.
53. Snoeyenbos-West, O.L., Nevin, K.P., Anderson, R.T., Lovley, D.R., 2000. Enrichment of Geobacter species in response to stimulation of Fe(III) reduction in sandy aquifer sediments. Microb. Ecol. 39, 153-167.
54. Summons, R.E., Jahnke, L.L., Roksandic, Z., 1994. Carbon isotopic fractionation in lipids from methanotrophic bacteria: relevance for interpretation of the geochemical record of biomarkers. Geochim. Cosmochim. Acta 58, 2853-2863.
55. Taylor, J., Parkes, R.J., 1983. The cellular fatty acids of the sulphate-reducing bacteria, Desulfobacter sp., Desulfobulbus sp., and Desulfovibrio desulfuricans. J. Gen. Microbiol. 129, 3303-3309.
56. Teece, M.A., Fogel, M.L., Dollhopf, M.E., Nealson, K.H., 1999. Isotopic fractionation associated with biosynthesis of fatty acids by a marine bacterium under oxic and anoxic conditions. Org. Geochem. 30, 1571-1579.
57. Truex, M.J., Peyton, B.M., Valentine, N.B., Gorby, Y.A., 1997. Kinetics of U(VI) reduction by a dissimilatory Fe(III)-reducing bacterium under non-growth conditions. Biotechnol. Bioeng. 55, 490-496.
58. Trüper, H.G., de' Clari, L., 1997. Taxonomic note: necessary correction of specific epithets formed as substantives (nouns) 'in apposition''. Int. J. Syst. Bacteriol. 47, 908-909.
59. Vainshtein, M., Hippe, H., Kroppenstedt, R.M., 1992. Cellular fatty acid composition of Desulfovibrio species and its use in classification of sulfate-reducing bacteria. Syst. Appl. Microbiol. 15, 554-566.
60. van der Meer, M.T.J., Schouten, S., Sinninghe Damsté, J.S., 1998. The effect of the reversed tricarboxylic-acid cycle on the C-13 contents of bacterial lipids. Org. Geochem. 28, 527-533.
61. van der Meer, M.T.J., Schouten, S., de Leeuw, J.W., Ward, D.M., 2000. Autotrophy of green non-sulphur bacteria in hot spring microbial mats: biological explanations for isotopically heavy organic carbon in the geological record. Environ. Microbiol. 2, 428-435.
62. 13C contents of organic components in the phototrophic bacterium Chloroflexus aurantiacus. J. Biol. Chem. 14, 10971-10976.
63. Venkateswaran, K., Moser, D.P., Dollhopf, M.E., Lies, D.P., Saffarini, D.A., MacGregor, B.J., Ringelberg, D.B., White, D.C., Nishijima, M., Sano, H., Burghardt, J., Stackebrandt, E., Nealson, K.H., 1999. Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov.. Int. J. Syst. Bacteriol. 49, 705-724.
64. White, D.C., 1988. Validation of quantitative analysis for microbial biomass, community structure, and metabolic activity. Adv. Limnol. 31, 1-18.
65. White, D.C., Davis, W.M., Nickels, J.S., King, J.D., Bobbie, R.J., 1979. Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 40, 51-62.
66. Zhang, C.L., 2002. Stable carbon isotopes of lipid biomarkers for analysis of metabolites and metabolic fates of environmental microorganisms. Curr. Opin. Biotechnol. 13, 25-30.
67. Zhang, C.L., Ye, Q., Reysenbach, A.-L., Goetz, D., Peacock, A., White, D.C., Horita, J., Cole, D.R., Fang, J., Pratt, L., Fang, J., Huang, Y., 2002. Carbon isotopic fractionations associated with thermophilic bacteria Thermotoga maritima and Persephonella marina. Environ. Microbiol. 4, 58-64.
68. Zhang, C.L., Li, Y., Wall, J.D., Larsen, L., Sassen, R., Huang, Y., Wang, Y., Peacock, A., White, D.C., Horita, J., Cole, D.R., 2002. Lipid and carbon isotopic evidence of methane-oxidizing and sulfate-reducing bacteria in association with gas hydrates from the Gulf of Mexico. Geology 30, 239-242.