Effects of iron and nitrogen limitation on sulfur isotope fractionation during microbial sulfate reduction

Applied and Environmental Microbiology

Volumn 78, Issue 23, 2012, Pages 8368-8376

  Sim, Min Sub ^a,b   Ono, Shuhei ^a   Bosak, Tanja ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONTROL CULTURES; DESULFOVIBRIO; ELECTRON ACCEPTOR; ELECTRON TRANSPORT CHAIN; IRON DEFICIENCY; NITROGEN LIMITATION; REDUCED NITROGEN; REDUCING POWER; SALT MARSHES; SULFATE REDUCING; SULFATE REDUCING BACTERIA; SULFATE REDUCTION; SULFUR ISOTOPE;

AMMONIUM COMPOUNDS; BACTERIA; CELL CULTURE; IRON; NITROGEN; NITROGEN FIXATION; SULFUR; SULFUR COMPOUNDS;

ISOTOPES;

BACTERIAL DNA; IRON; NITROGEN; SULFATE; SULFUR;

CYTOCHROME; IRON; ISOTOPIC FRACTIONATION; NITROGEN; NITROGEN FIXATION; SALTMARSH; SULFATE-REDUCING BACTERIUM; SULFUR ISOTOPE;

ARTICLE; CHEMISTRY; DESULFOVIBRIO; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; ISOTOPE LABELING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION;

DESULFOVIBRIO; DNA, BACTERIAL; ENVIRONMENTAL MICROBIOLOGY; IRON; ISOTOPE LABELING; MOLECULAR SEQUENCE DATA; NITROGEN; OXIDATION-REDUCTION; SEQUENCE ANALYSIS, DNA; SULFATES; SULFUR ISOTOPES;

CAPE COD; MASSACHUSETTS; UNITED STATES;

BACTERIA (MICROORGANISMS); DESULFOVIBRIO;

EID: 84870772382     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01842-12     Document Type: Article

References (69)

1. Adams DD, Hurtgen MT, Sageman BB. 2010. Volcanic triggering of a biogeochemical cascade during Oceanic Anoxic Event 2. Nat. Geosci. 3:201-204.
2. Alkan N, Tüfekçi M. 2009. Distribution of dissolved forms of manganese and iron in the water column of the southeastern Black Sea. Turk. J. Fish. Aquat. Sci. 9:159 -164.
3. Anderson TR, Pondaven P. 2003. Non-redfield carbon and nitrogen cycling in the Sargasso Sea: pelagic imbalance and export flux. Deep Sea Res. I 50:573-591.
4. Bertics VJ, et al. 2012. Occurrence of benthic microbial nitrogen fixation coupled to sulfate reduction in the seasonally hypoxic Eckernförde Bay, Baltic Sea. Biogeosciences 9:6489-6533.
5. Bevington PR, Robinson DK. 2003. Data reduction and error analysis for the physical sciences, 3rd ed. McGraw-Hill, New York, NY.
6. Bolliger C, Schroth MH, Bernasconi SM, Kleikemper J, Zeyer J. 2001. Sulfur isotope fractionation during microbial sulfate reduction by toluene-degrading bacteria. Geochim. Cosmochim. Acta 19:3289 -3298.
7. Böttcher ME, et al. 2000. The biochemistry, stable isotope geochemistry, and microbial community structure of a temperate intertidal mudflat: an integrated study. Cont. Shelf Res. 20:1749 -1769.
8. Bottrell SH, Newton R. 2006. Reconstruction of change in global sulfur cycling from marine sulfate isotopes. Earth Sci. Rev. 75:59-83.
9. Brunner B, Bernasconi SM. 2005. A revised isotope fractionation model for dissimilatory sulfate reduction in sulfate reducing bacteria. Geochim. Cosmochim. Acta 69:4759-4771.
10. Burgess BK. 1990. The iron-molybdenum cofactor of nitrogenase. Chem. Rev. 90:1377-1406.
11. Calvert SE, Karlin RE. 1991. Relationships between sulphur, organic carbon, and iron in the modern sediments of the Black Sea. Geochim. Cosmochim. Acta 55:2483-2490.
12. Canfield DE, Farquhar J, Zerkle AL. 2010. High isotope fractionations during sulfate reduction in a low-sulfate euxinic ocean analog. Geology 38:415- 418.
13. Canfield DE, Raiswell R. 1999. The evolution of the sulfur cycle. Am. J. Sci. 299:679 -723.
14. Chambers LA, Trudinger PA. 1979. Microbiological fractionation of stable sulfur isotopes: a review and critique. Geomicrobiol. J. 1:249 -293.
15. Chambers LA, Trudinger PA, Smith JW, Burns MS. 1975. Fractionation of sulfur isotopes by continuous cultures of Desulfovibrio desulfuricans. Can. J. Microbiol. 21:1602-1607.
16. Cline JD. 1969. Spectrophotometric determination of hydrogen sulfide in natural water. Limnol. Oceanogr. 14:454-458.
17. Cotter PA, Darie S, Gunsalus RP. 1992. The effect of iron limitation on expression of the aerobic and anaerobic electron transport pathway genes in Escherichia coli. FEMS Microbiol. Lett. 79:227-232.
18. Davison W. 1991. The solubility of iron sulphides in synthetic and natural water at ambient temperature. Aquat. Sci. 53:309 -329.
19. Del Don C, Hanselmann KW, Peduzzi R, Bachofen R. 2001. The meromictic alpine Lake Cadagno: orographical and biochemical description. Aquat. Sci. 63:70 -90.
20. Detmers J, Bruchert V, Habicht K, Kuever J. 2001. Diversity of sulfur isotope fractionations by sulfate reducing prokaryotes. Appl. Environ. Microbiol. 67:888-894.
21. Dilworth MJ. 1966. Acetylene reduction by nitrogen-fixing preparations from Clostridium pasteurianum. Biochim. Biophys. Acta 127:285-294.
22. Dwyer DF, Weeg-Aerssens E, Shelton DR, Tiedje JM. 1988. Bioenergetic conditions of butyrate metabolism by a syntrophic, anaerobic bacterium in coculture with hydrogen-oxidizing methanogenic and sulfidogenic bacteria. Appl. Environ. Microbiol. 54:1354 -1359.
23. Farquhar J, et al. 2003. Multiple sulphur isotopic interpretations of biosynthetic pathways: implications for biological signatures in the sulphur isotope record. Geobiology 1:27-36.
24. Fulweiler RW, Nixon SW, Buckley BA, Granger SL. 2007. Reversal of the net dinitrogen gas flux in coastal marine sediments. Nature 448:180 -182.
25. Gavel OY, et al. 1998. ATP sulfurylases from sulfate-reducing bacteria of the genus Desulfovibrio. A novel metalloprotein containing cobalt and zinc. Biochemistry 37:16225-16232.
26. Giblin AE, Howarth RW. 1984. Porewater evidence for a dynamic sedimentary iron cycle in salt marshes. Limnol. Oceanogr. 29:47- 63.
27. Habicht KS, Gabe M, Thamdrup B, Berg P, Canfield DE. 2002. Calibration of sulfate levels in the Archean ocean. Science 298:2372-2374.
28. Habicht KS, Salling L, Thamdrup B, Canfield DE. 2005. Effect of low sulfate concentrations on lactate oxidation and isotope fractionation during sulfate reduction by Archaeoglobus fulgidus strain Z. Appl. Environ. Microbiol. 71:3770 -3777.
29. Halm H, et al. 2009. Co-occurrence of denitrification and nitrogen fixation in a meromictic lake, Lake Cadagno (Switzerland). Environ. Microbiol. 11:1945-1958.
30. Handley KH, Boothman C, Mills RA, Pancost RD, Lloyd JR. 2010. Functional diversity of bacteria in a ferruginous hydrothermal sediment. ISME J. 4:1193-1205.
31. Harder W, Dijkhuizen L. 1983. Physiological responses to nutrient limitation. Annu. Rev. Microbiol. 37:1-23.
32. Harrison AG, Thode HG. 1958. Mechanism of the bacterial reduction of sulphate from isotope fractionation studies. Trans. Faraday Soc. 54:84 -92.
33. Herbert RB, Jr, Benner SG, Pratt AR, Blowes DW. 1998. Surface chemistry and morphology of poorly crystalline iron sulfides precipitated in media containing sulfate-reducing bacteria. Chem. Geol. 144:87-97.
34. Hetzel A, Böttcher ME, Wortmann UG, Brumsack H-J. 2009. Paleoredox conditions during OAE2 reflected in Demerara Rise sediment geochemistry (ODP Leg 207). Palaeogeogr. Palaeoclimatol. Palaeoecol. 273: 302-328.
35. Hines ME, Bazylinski DA, Tugel JB, Lyons WB. 1991. Anaerobic microbial biogeochemistry in sediments from two basins in the Gulf of Maine: evidence for iron and manganese reduction. Estuar. Coast. Shelf Sci. 32:313-324.
36. Holmes RM, Aminot A, Kerouel R, Hooker BA, Peterson BJ. 1999. A simple and precise method for measuring ammonium in marine and fresh water ecosystems. Can. J. Fish. Aquat. Sci. 56:1801-1808.
37. Hubbard JAM, Lewandowska KB, Hughes MN, Poole RK. 1986. Effects of iron-limitation of Escherichia coli on growth, the respiratory chains and gallium uptake. Arch. Microbiol. 146:80-86.
38. Johnston WA, Huang W, de Voss JJ, Hayes MA, Gillam EM. 2008. Quantitative whole-cell cytochrome P450 measurement suitable for highthroughput application. J. Biomol. Screen. 13:135-141.
39. Jones GA, Pickard MD. 1980. Effect of titanium (III) citrate as reducing agent on growth of rumen bacteria. Appl. Environ. Microbiol. 39:1144- 1147.
40. Kaplan IR, Rittenberg SC. 1964. Microbiological fractionation of sulphur isotopes. J. Gen. Microbiol. 34:195-212.
41. Keller KL, Wall JD. 2011. Genetics and molecular biology of the electron flow for sulfate respiration in Desulfovibrio. Front. Microbiol. 2:135.
42. King GM, Klug MJ, Wiegert RG, Chalmers AG. 1982. Relation of soil water movement and sulfide concentration to Spartina alterniflora production in a Georgia salt marsh. Science 218:61- 63.
43. Kleikemper J, et al. 2002. Activity and diversity of sulfate-reducing bacteria in a petroleum hydrocarbon-contaminated aquifer. Appl. Environ. Microbiol. 68:1516 -1523.
44. Kremer DR, Nienhuis-Kuiper HE, Timmer CJ, Hansen TA. 1989. Catabolism of malate and related dicarboxylic acids in various Desulfovibrio strains and the involvement of an oxygen-labile NADPH dehydrogenase. Arch. Microbiol. 151:34 -39.
45. Lamperia J, Pereira AS, Moura JJG. 1994. Adenylylsulfate reductase from sulfate-reducing bacteria. Methods Enzymol. 243:241-260.
46. Lewis BL, Landing WM. 1991. The biogeochemistry of manganese and iron in the Black Sea. Deep Sea Res. 38:S773-S803.
47. Meyer KM, Kump LR. 2008. Oceanic euxinia in Earth history: causes and consequences. Annu. Rev. Earth Planet. Sci. 36:251-288.
48. Moreau JW, Zierenberg RA, Banfield JF. 2010. Diversity of dissimilatory sulfate reductase genes (dsrAB) in a salt marsh impacted by long-term acid mine drainage. Appl. Environ. Microbiol. 76:4819-4828.
49. Odom JM, Peck HD, Jr. 1981. Hydrogen cycling as a general mechanism for energy coupling in the sulfate reducing bacteria, Desulfovibrio sp. FEMS Microbiol. Lett. 12:47-50.
50. O'Leary MH. 1989. Multiple isotope effects on enzyme-catalyzed reactions. Annu. Rev. Biochem. 58:377- 401.
51. Ono S, Keller NS, Rouxel O, Alt J. 2012. Sulfur-33 cosnstraints on the origin of secondary pyrite in altered oceanic basement. Geochim. Cosmochim. Acta 87:323-340.
52. Ono S, Wing B, Rumble D, Farquhar J. 2006. High precision analysis of all four stable isotope of sulfur (32S, 33S, 34S and 36S) at nanomole levels using a laser fluorination isotope-ratio-monitoring gas chromatography-mass spectrometry. Chem. Geol. 225:30 -39.
53. Pagni M, Beffa T, Isch C, Aragno M. 1992. Linear growth and poly (-hydroxybutyrate) synthesis in response to pulse-wise addition of the growth-limiting substrate to steady-state heterotrophic continuous cultures of Aquaspirillum autotrophicum. J. Gen. Microbiol. 138:429-436.
54. Pereira IAC, et al. 2011. A comparative genomic analysis of energy metabolism in sulfate reducing bacteria and archaea. Front. Microbiol. 2:69.
55. Postgate JR. 1956. Iron and synthesis of cytochrome c3. J. Gen. Microbiol. 15:186 -193.
56. Postgate JR. 1982. The fundamental of nitrogen fixation. Cambridge University Press, Cambridge, United Kingdom.
57. Postgate JR, Campbell LL. 1966. Classification of Desulfovibrio species, the non-sporulating sulfate-reducing bacteria. Bacteriol. Rev. 30:732-738.
58. Rabus R, Hansen TA, Widdel F. 2006. Dissimilatory sulfate- and sulfurreducing prokaryotes, p 659-786. In Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackbrandt E (ed), The prokaryotes. Springer-Verlag, New York, NY.
59. Rees CE. 1973. A steady-state model for sulphur isotope fractionation in bacterial reduction processes. Geochim. Cosmochim. Acta 37:1141-1162.
60. Rickard D, Luther GW, III. 2007. Chemistry of iron sulfides. Chem. Rev. 107:514 -562.
61. Rudnicki MD, Elderfield H, Spiro B. 2001. Fractionation of sulfur isotopes during bacterial sulfate reduction in deep ocean sediments at elevated temperatures. Geochim. Cosmochim. Acta 65:777-789.
62. Sim MS, Ono S, Donovan K, Templer SP, Bosak T. 2011. Effect of electron donors on the fractionation of sulfur isotopes by a marine Desulfovibrio sp. Geochim. Cosmochim. Acta 75:4244-4259.
63. Sim MS, Bosak T, Ono S. 2011. Large sulfur isotope fractionation does not require disproportionation. Science 333:74 -77.
64. Stams FJM, Veenhuis M, Weenk GH, Hanssen TA. 1983. Occurrence of polyglucose as a storage polymer in Desulfovibrio species and Desulfobulbus propionicus. Arch. Microbiol. 136:54 -59.
65. Sweeny RE, Kaplan IR. 1980. Stable isotope composition of dissolved sulfate and hydrogen sulfide in the Black Sea. Mar. Chem. 9:145-152.
66. Thode HG, Monster J, Dunford HB. 1961. Sulphur isotope geochemistry. Geochim. Cosmochim. Acta 25:158 -174.
67. Wang G, Spivack AJ, D'Hondt S. 2010. Gibbs energies of reaction and microbial mutualism in anaerobic deep subseafloor sediments ofODPsite 1226. Geochim. Cosmochim. Acta 74:3938 -3947.
68. Widdel F, Kohring GW, Mayer F. 1983. Studies on dissimilatory sulfatereducing bacteria that decomposed fatty acids. III. Characterization of the filamentous gliding Desulfonema limocola gen. nov. sp. nov. and Desulfonema magnum sp. nov. Arch. Microbiol. 134:286 -294.
69. Wright RT, Coffin RB. 1984. Measuring microzooplankton grazing on planktonic marine bacteria by its impact on bacterial production. Microb. Ecol. 10:137-149.