Microbial stable isotope fractionation of mercury: A synthesis of present understanding and future directions

Chemical Geology

Volumn 336, Issue , 2013, Pages 13-25

  Kritee, K ^a   Blum, Joel D ^b   Reinfelder, John R ^a   Barkay, Tamar ^a  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Enzyme level isotope effect; Isotope; Mass dependent fractionation; Mercury; Microbial multi step processes

Indexed keywords

ECOSYSTEM LEVELS; ENVIRONMENTAL SAMPLE; EXPERIMENTAL DETERMINATION; FOOD CHAIN; FRACTIONATION FACTORS; HEALTH CONSEQUENCES; ISOTOPE EFFECT; ISOTOPIC FRACTIONATIONS; KINETICALLY CONTROLLED; MICROBIAL TRANSFORMATION; MONOMETHYLMERCURY; MULTI-STEP; STABLE ISOTOPES; THEORETICAL CALCULATIONS; TRACE METAL;

ECOLOGY; ISOTOPES; ITERATIVE METHODS; PROCESS CONTROL;

MERCURY (METAL);

ENZYME ACTIVITY; ISOTOPIC FRACTIONATION; MERCURY (ELEMENT); PUBLIC HEALTH; STABLE ISOTOPE; TRACE METAL;

EID: 84871929054     PISSN: 00092541     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chemgeo.2012.08.017     Document Type: Article

References (86)

1. Aller A.J., Lumbreras J.M., Robles L.C., Fernández G.M. Stability of bacterium-mercury complexes and speciation of soluble inorganic mercury species. Analytica Chimica Acta 1996, 330(1):89-105.
2. Apontoweil P., Berends W. Isolation and initial characterization of glutathione-deficient mutants of Escherichia coli K12. Biochimica et Biophysica Acta 1975, 399(1):10-22.
3. Barkay T., Wagner-Dobler I. Microbial transformations of mercury: potentials, challenges, and achievements in controlling mercury toxicity in the environment. Advances in Applied Microbiology 2005, 57:1-52.
4. Barkay T., Gillman M., Turner R.R. Effects of dissolved organic carbon and salinity on bioavailability of mercury. Applied and Environmental Microbiology 1997, 63(11):4267-4271.
5. Barkay T., Miller S.M., Summers A.O. Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiology Reviews 2003, 27:355-384.
6. Barkay T., Kritee K., Boyd E., Geesey G. A thermophilic bacterial origin and subsequent constraints by redox, light and salinity on the evolution of the microbial mercuric reductase. Environmental Microbiology 2010, 12(11):2904-2917.
7. Beard B.L., et al. Iron isotope biosignatures. Science 1999, 285(5435):1889-1892.
8. Begley T.P., Walts A.E., Walsh C.T. Bacterial organomercurial lyase: overproduction, isolation, and characterization. Biochemistry 1986, 25(22):7186-7192.
9. Bergquist B.A., Blum J.D. Mass-dependent and mass-independent fractionation of Hg isotopes by photo-reduction in aquatic systems. Science 2007, 318(5849):417-420.
10. Bergquist B.A., Blum J.D. The odds and evens of mercury isotopes: applications of mass-dependent and mass-independent isotope fractionation. Elements 2009, 5(6):353-357.
11. Bigeleisen J. The relative velocities of isotopic molecules. The Journal of Chemical Physics 1949, 17(8):675-678.
12. Blum J.D. Applications of stable mercury isotopes to biogeochemistry. Handbook of Environmental Isotope Geochemistry 2011, 229-246. Springer. M. Baskaran (Ed.).
13. Blum J.D., Bergquist B.A. Reporting of variations in the natural isotopic composition of mercury. Analytical and Bioanalytical Chemistry 2007, 388(2):353-359.
14. Brunner B., Bernasconi S.M. A revised isotope fractionation model for dissimilatory sulfate reduction in sulfate reducing bacteria. Geochimica et Cosmochimica Acta 2005, 69(20):4759-4771.
15. Buchachenko A., et al. Magnetic isotope effect for mercury nuclei in photolysis of bis(p-trifluoromethylbenzyl) mercury. Doklady Physical Chemistry 2007, 413(1):39-41.
16. Canfield D.E. Biogeochemistry of sulfur isotopes. Stable Isotope Geochemistry 2001, The Mineralogical Society of America, Washington, DC. J.W. Valley, D.R. Cole (Eds.).
17. Canfield D.E. Isotope fractionation by natural populations of sulfate-reducing bacteria. Geochimica et Cosmochimica Acta 2001, 65(7):1117-1124.
18. Cook P.F. Enzyme mechanism from isotope effects 1991, CRC Press, Inc., Florida.
19. 3 as an example. Planta 2001, 214(2):220-234.
20. Das R., Odom L.A. In vivo mass-independent fractionation of mercury isotopes in fish. Eos Trans. AGU, Fall meet. Suppl., Abstract V52B-07 2008, 89(53).
21. Daughney C.J., Siciliano S.D., Rencz A.N., Lean D., Fortin D. Hg(II) adsorption by bacteria: a surface complexation model and its application to shallow acidic lakes and wetlands in Kejimkujik National Park, Nova Scotia, Canada. Environmental Science and Technology 2002, 36(7):1546-1553.
22. Dzurko M. Fractionation of mercury isotopes during methylation by sulfate-reducing bacteria (Abstract S-668). 8th International Conference on Mercury as a Global Pollutant 2006, 109.
23. Estrade N., Carignan J., Sonke J.E., Donard O.F.X. Mercury isotope fractionation during liquid-vapor evaporation experiments. Geochimica et Cosmochimica Acta 2009, 73(10):2693-2711.
24. Fitzgerald W.F., Lamborg C.H., Hammerschmidt C.R. Marine biogeochemical cycling of mercury. Chemical Reviews 2007, 107(2):641-662.
25. Fleming E.J., Mack E.E., Green P.G., Nelson D.C. Mercury methylation from unexpected sources: molybdate-inhibited freshwater sediments and an iron-reducing bacterium. Applied and Environmental Microbiology 2006, 72:457-464.
26. Foucher D., Ogrinc N., Hintelmann H. Tracing mercury contamination from the Idrija Mining Region (Slovenia) to the Gulf of Trieste using Hg isotope ratio measurements. Environmental Science and Technology 2008, 43:33-39.
27. Galimov E.M. The Biological Fractionation of Isotopes 1985, Academic Press, Inc., Orlando, Florida, 261pp.
28. Ghosh S., Sadhukhan P.C., Chaudhuri J., Ghosh D.K., Mandal A. Purification and properties of mercuric reductase from Azotobacter chroococcum. Journal of Applied Microbiology 1999, 86:7-12.
29. Ghosh S., Xu Y., Humayun M., Odom L. Mass-independent fractionation of mercury isotopes in the environment 9, Q03004. Geochemistry, Geophysics, Geosystems 2008, 9. 10.1029/2007GC001827.
30. Granger J., Sigman D.M., Lehmann M.F., Tortell P.D. Nitrogen and oxygen isotope fractionation of during dissimilatory nitrate reduction by denitrifying bacteria. Limnology and Oceanography 2008, 53(6):2533-2545.
31. Grissom C.B. Magnetic field effects in biology: a survey of possible mechanisms with emphasis on radical-pair recombination. Chemical Reviews 1995, 95(1):3-24.
32. Hammerschmidt C.R., Fitzgerald W.F., Lamborg C.H., Balcom P.H., Tseng C.M. Biogeochemical cycling of methylmercury in lakes and tundra watersheds of Arctic Alaska. Environmental Science and Technology 2006, 40:1204-1211.
33. Hoefs J. Stable Isotope Geochemistry 2004, Springer-Verlag, Berlin Heidelberg.
34. Honig B.H., Hubbell W.L., Flewelling R.F. Electrostatic interactions in membranes and proteins. Annual Review of Biophysics and Biophysical Chemistry 1986, 15(1):163-193.
35. Huang C.-C., Narita M., Yamagata T., Endo G. Identification of three MerB genes and characterization of a broad-spectrum mercury resistance module encoded by a class II transposon of Bacillus megaterium strain MB1. Gene 1999, 239(2):361-366.
36. Inouea C., Sugawaraa K., Kusano T. Thiobacillus ferrooxidans mer operon: sequence analysis of the promoter and adjacent genes. Gene 1990, 96:115-120.
37. 2-inducible polypeptides encoded by the mer operon of plasmid R100. Journal of Bacteriology 1982, 151(2):962-970.
38. Jackson T.A., Whittle D.M., Evans M.S., Muir D.C.G. Evidence for mass-independent and mass-dependent fractionation of the stable isotopes of mercury by natural processes in aquatic ecosystems. Applied Geochemistry 2008, 33(3):547-571.
39. Jing Y.D., He Z.L., Yang X.E. Adsorption-desorption characteristics of mercury in paddy soils of China. Journal of Environmental Quality 2008, 37(2):680-688.
40. Johnson T.M., Bullen T.D. Mass-dependent fractionation of selenium and chromium isotopes in low temperature environments. Geochemistry of Non-traditional Stable Isotopes 2004, The Mineralogical Society of America, Washington, DC. C.M. Johnson, B.L. Beard, F. Albarede (Eds.).
41. Kerin E.J., et al. Mercury methylation by dissimilatory iron-reducing bacteria. Applied and Environmental Microbiology 2006, 72:7919-7921.
42. Koster van Groos P.G., Esser B.K., Willians R., Hunt J.R. Mercury isotope fractionation due to permeation of a PVC polymer. Geochimica et Cosmochimica Acta 2009, 73(13):A687.
43. Kritee K. Mass Independent fractionation of mercury and microbiology: where can they intersect?. Geochimica et Cosmochimica Acta 2010, 74(1):A541.
44. Kritee K., Blum J.D., Johnson M.W., Bergquist B.A., Barkay T. Mercury stable isotope fractionation during reduction of Hg(II) to Hg(0) by mercury resistant microorganisms. Environmental Science and Technology 2007, 41(6):1889-1895.
45. Kritee K., Blum J.D., Barkay T. Mercury stable isotope fractionation during reduction of Hg(II) to Hg(0) by different microbial pathways. Environmental Science and Technology 2008, 42(24):9171-9177.
46. Kritee K., Barkay T., Blum J.D. Mass dependent mercury stable isotope fractionation during mer mediated microbial degradation of monomethylmercury. Geochimica et Cosmochimica Acta 2009, 73(5):1285-1296.
47. 2+ from proteins, delivers it to the catalytic core, and protects cells under glutathione-depleted conditions. Biochemistry 2005, 44(34):11402-11416.
48. Lewis B.E., Schramm V.L. Enzymatic binding isotope effects and the interaction of glucose with hexokinase. Isotope Effects in Chemistry and Biology 2006, 1020-1048. Taylor and Francis Group, Florida. A. Kohen, H. Limbach (Eds.).
49. Liao X.-Y., Shen W., Chen J., Li Y., Du G.-C. Improved glutathione production by gene expression in Escherichia coli. Letters in Applied Microbiology 2006, 43(2):211-214.
50. Lin C.-C., Yee N., Barkay T. Microbial transformation in the mercury cycle. Environmental Chemistry and Toxicology of Mercury 2011, John Wiley & Sons, Inc., Hoboken, NJ, USA. 10.1002/9781118146644.ch5. G. Liu, Y. Cai, N. O'Driscoll (Eds.).
51. Lindberg S., et al. A synthesis of progress and uncertainties in attributing the sources of mercury in deposition. Ambio 2007, 36(1):19-32.
52. Malinovsky D., Vanhaecke F. Mercury isotope fractionation during abiotic transmethylation reactions. International Journal of Mass Spectrometry 2011, 307:214-224.
53. Mason R.P., Sheu G.-R. Role of the ocean in the global mercury cycle. Global Biogeochemical Cycles 2002, 16(4):1093-2007.
54. Mason R.P., Morel F.M.M., Hemond H.F. The role of microorganisms in elemental mercury formation in natural waters. Water, Air, and Soil Pollution 1995, 80:775-787.
55. Melander L. Isotope Effects on Reaction Rates 1960, The Ronald Press Company, New York.
56. Miller S.M. Bacterial detoxification of Hg(II) and organomercurials. Essays in Biochemistry 1999, 14-30. Portland Press, London. D.P. Ballou (Ed.).
57. Morel F.M.M., Kraepiel A.M.L., Amyot M. The chemical cycle and bioaccumulation of mercury. Annual Review of Ecology and Systematics 1998, 29:543-566.
58. Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiology and Molecular Biology Reviews 2003, 67(4):593-656.
59. Perrot V., et al. Evaluation of species-specific mercury isotopic fractionation during biotic and abiotic methylation. The 10th International Conference on Mercury as a Global Pollutant, Halifax, Canada 2011.
60. Pinto E., et al. Heavy metal induced oxidative stress in algae. Journal of Phycology 2003, 39(6):1008-1018.
61. Pitts K.E., Summers A.O. The roles of thiols in the bacterial organomercurial lyase (MerB). Biochemistry 2002, 41(32):10287-10296.
62. Rasmussen L.D., Turner R.R., Barkay T. Cell-density-dependent sensitivity of a mer-lux bioassay. Applied and Environmental Microbiology 1997, 63(8):3291-3293.
63. Rees C.E. A steady state model for sulfur isotope fractionation in bacterial reduction processes. Geochimica et Cosmochimica Acta 1973, 37:1141-1162.
64. Richter F.M., et al. Kinetic isotopic fractionation during diffusion of ionic species in water. Geochimica et Cosmochimica Acta 2006, 70(2):277-289.
65. Ridley W.I., Stetson S.J. A review of isotopic composition as an indicator of the natural and anthropogenic behavior of mercury. Applied Geochemistry 2006, 21(11):1889-1899.
66. Rodriguez-Gonzalez P., et al. Species-specific stable isotope fractionation of mercury during Hg(II) methylation by an anaerobic bacteria (Desulfobulbus propionicus) under dark conditions. Environmental Science and Technology 2009, 43(24):9183-9188.
67. Rodushkin I., Stenberg A., Andren H., Malinovsky D., Baxter D.C. Isotopic fractionation during diffusion of transition metal ions in solution. Analytical Chemistry 2004, 76(7):2148-2151.
68. Sahlman L., Wong W., Powlowski J. A mercuric ion uptake role for the integral inner membrane protein, MerC, involved in bacterial mercuric ion resistance. Journal of Biological Chemistry 1997, 272:29518-29526.
69. Schaefer J.K., Morel F.M.M. High methylation rates of mercury bound to cysteine by Geobacter sulfurreducens. Nature Geoscience 2009, 2(2):123-126.
70. Schaefer J.K., et al. The role of the bacterial organomercury lyase (MerB) in controlling methylmercury accumulation in mercury contaminated natural waters. Environmental Science and Technology 2004, 38:4304-4311.
71. Schauble E.A. Applying stable isotope fractionation theory to new systems. Reviews in Minerology & Geochemistry 2004, 65-111. The Mineralogical Society of America, Washington. C.M. Johnson, B.L. Beard, F. Albarède (Eds.).
72. Schauble E.A. Role of nuclear volume in driving equilibrium stable isotope fractionation of mercury, thallium, and other very heavy elements. Geochimica et Cosmochimica Acta 2007, 71(9):2170-2189.
73. Scott K.M., Lu X., Cavanaugh C.M., Lu J.S. Optimal methods for estimating kinetic isotope effects from different forms of the Raleigh distillation equation. Geochimica et Cosmochimica Acta 2004, 68:433-442.
74. Shiratori T. Cloning and expression of Thiobacillus ferrooxidans mercury ion resistance genes in Escherichia coli. Journal of Bacteriology 1989, 171(171):3458-3464.
75. Skogerboe R.K., Wilson S.A. Reduction of ionic species by fulvic acid. Analytical Chemistry 1981, 53:228-232.
76. Skulan J.L., Beard B.L., et al. Kinetic and equilibrium Fe isotope fractionation between aqueous Fe(III) and hematite. Geochimica et Cosmochimica Acta 2002, 66(17):2995-3015.
77. Valley J.W., Cole D.R. Stable Isotope Geochemistry. The Mineralogical Society of America 2001, Washington, DC.
78. Wiatrowski H.A., Ward P.M., Barkay T. Novel reduction of mercury(II) by mercury-sensitive dissimilatory metal reducing bacteria. Environmental Science and Technology 2006, 40(21):6690-6696.
79. Wiederhold J.G., et al. Equilibrium mercury isotope fractionation between dissolved Hg(II) species and thiol-bound Hg. Environmental Science and Technology 2010, 44(11):4191-4197.
80. Wilson J.R., Leang C., Morby A.P., Hobman J.L., Brown N.L. MerF is a mercury transport protein: Different structures but a common mechanism for mercuric ion transporters?. FEBS Letters 2000, 472(1):78-82.
81. Yates L.M., von Wandruszka R. Functional group analysis of Suwannee River fulvic acid with reactive fluorescent probes. Fresenius Journal of Analytical Chemistry 1999, 364(8):746-748.
82. Yin Y., Allen H.E., Huang C.P., Sparks D.L., Sanders P.F. Kinetics of mercury(II) adsorption and desorption on soil. Environmental Science and Technology 1997, 31(2):496-503.
83. Yin R., Feng X., Shi W. Application of the stable-isotope system to the study of sources and fate of Hg in the environment: a review. Applied Geochemistry 2010, 25(10):1467-1477.
84. Zheng W., Hintelmann H. Mercury isotope fractionation during photoreduction in natural water is controlled by its Hg/DOC ratio. Geochimica et Cosmochimica Acta 2009, 73(22):6704-6715.
85. Zheng W., Hintelmann H. Isotope fractionation of mercury during its photochemical reduction by low-molecular-weight organic compounds. Journal of Physical Chemistry A 2010, 114(12):4246-4253.
86. Zheng W., Hintelmann H. Nuclear field shift effect in isotope fractionation of mercury during abiotic reduction in the absence of light. Journal of Physical Chemistry A 2010, 114(12):4238-4245.