Effect of dissolved organic matter source and character on microbial Hg methylation in Hg-S-DOM solutions

Environmental Science and Technology

Volumn 47, Issue 11, 2013, Pages 5746-5754

  Graham, Andrew M ^a,b   Aiken, George R ^c   Gilmour, Cynthia C ^b  

^a GRINNELL COLLEGE   (United States)

^b SMITHSONIAN ENVIRONMENTAL RESEARCH CENTER   (United States)

^c U S GEOLOGICAL SURVEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DESULFOVIBRIO DESULFURICANS; DISSOLVED ORGANIC MATTERS; FATE AND TRANSPORT; HIGH MOLECULAR WEIGHT; HIGH SULFUR CONTENTS; MERCURIES (HG); SULFIDE CONCENTRATION;

ALKYLATION; BACTERIA; BIOCHEMISTRY; BIOLOGICAL MATERIALS; EXPERIMENTS; MERCURY COMPOUNDS; METHYLATION; SULFUR COMPOUNDS;

MERCURY (METAL);

DISSOLVED ORGANIC MATTER; MERCURY; NANOPARTICLE; SULFUR;

BIOASSAY; BIOAVAILABILITY; DISSOLVED ORGANIC MATTER; MERCURY (ELEMENT); MICROBIAL COMMUNITY; SUPERSATURATION; TRANSPORT PROCESS;

ARTICLE; BACTERIAL GROWTH; BIOAVAILABILITY; CELL ASSAY; DESULFOVIBRIO DESULFURICANS; METHYLATION; MOLECULAR WEIGHT; NONHUMAN;

DESULFOVIBRIO DESULFURICANS; ECOSYSTEM; HUMIC SUBSTANCES; MERCURY; METHYLATION; NANOPARTICLES; SULFIDES;

BACTERIA (MICROORGANISMS); DESULFOVIBRIO DESULFURICANS;

EID: 84878664788     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es400414a     Document Type: Article

References (59)

1. Benoit, J.; Mason, R.; Gilmour, C.; Aiken, G. Constants for mercury binding by dissolved organic matter isolates from the Florida Everglades Geochim. Cosmochim. Acta 2001, 65, 4445-4451 (Pubitemid 34045961)
2. Haitzer, M.; Aiken, G.; Ryan, J. Binding of mercury(II) to dissolved organic matter: The role of the mercury-to-DOM concentration ratio Environ. Sci. Technol. 2002, 36, 3564-3570 (Pubitemid 35215184)
3. Haitzer, M.; Aiken, G.; Ryan, J. Binding of mercury(II) to aquatic humic substances: Influence of pH and source of humic substances Environ. Sci. Technol. 2003, 37, 2436-2441 (Pubitemid 36644751)
4. Lamborg, C.; Tseng, C.; Fitzgerald, W.; Balcom, P.; Hammerschmidt, C. Determination of the mercury complexation characteristics of dissolved organic matter in natural waters with "reducible Hg" titrations Environ. Sci. Technol. 2003, 37, 3316-3322 (Pubitemid 36935631)
5. Han, S.; Gill, G. Determination of mercury complexation in coastal and estuarine waters using competitive ligand exchange method Environ. Sci. Technol. 2005, 39, 6607-6615 (Pubitemid 41266143)
6. Schuster, P. F.; Striegl, R. G.; Aiken, G. R.; Krabbenhoft, D. P.; Dewild, J. F.; Butler, K.; Kamark, B.; Dornblaser, M. Mercury export from the Yukon River Basin and potential response to a changing climate Environ. Sci. Technol. 2011, 45, 9262-9267
7. Bergamaschi, B. A.; Krabbenhoft, D. P.; Aiken, G. R.; Patino, E.; Rumbold, D. G.; Orem, W. H. Tidally driven export of dissolved organic carbon, total mercury, and methylmercury from a mangrove-dominated estuary Environ. Sci. Technol. 2012, 46, 1371-1378
8. Khwaja, A. R.; Bloom, P. R.; Brezonik, P. L. Binding strength of methylmercury to aquatic NOM Environ. Sci. Technol. 2010, 44, 6151-6156
9. Dong, W.; Liang, L.; Brooks, S.; Southworth, G.; Gu, B. Roles of dissolved organic matter in the speciation of mercury and methylmercury in a contaminated ecosystem in Oak Ridge, Tennessee Environ. Chem. 2010, 7, 94-102
10. Mitchell, C. P. J.; Jordan, T. E.; Heyes, A.; Gilmour, C. C. Tidal exchange of total mercury and methylmercury between a salt marsh and a Chesapeake Bay sub-estuary Biogeochemistry 2012, 111 (1-3) 583-600
11. Ravichandran, M.; Aiken, G.; Ryan, J.; Reddy, M. Inhibition of precipitation and aggregation of metacinnabar (mercuric sulfide) by dissolved organic matter isolated from the Florida Everglades Environ. Sci. Technol. 1999, 33, 1418-1423 (Pubitemid 29217826)
12. Deonarine, A.; Hsu-Kim, H. Precipitation of mercuric sulfide nanoparticles in NOM-containing water: Implications for the natural environment Environ. Sci. Technol. 2009, 43, 2368-2373
13. Slowey, A. J. Rate of formation and dissolution of mercury sulfide nanoparticles: The dual role of natural organic matter Geochim. Cosmochim. Acta 2010, 74, 4693-4708
14. Gerbig, C.; Kim, C.; Stegemeier, J.; Ryan, J. N.; Aiken, G. R. Formation of nanocolloidal metacinnabar in mercury-DOM-sulfide systems Environ. Sci. Technol. 2011, 45, 9180-9187
15. Ravichandran, M.; Aiken, G.; Reddy, M.; Ryan, J. Enhanced dissolution of cinnabar (mercuric sulfide) by dissolved organic matter isolated from the Florida Everglades Environ. Sci. Technol. 1998, 32, 3305-3311 (Pubitemid 28503496)
16. Waples, J.; Nagy, K.; Aiken, G.; Ryan, J. Dissolution of cinnabar (HgS) in the presence of natural organic matter Geochim. Cosmochim. Acta 2005, 69, 1575-1588 (Pubitemid 40426677)
17. Barkay, T.; Gillman, M.; Turner, R. Effects of dissolved organic carbon and salinity on bioavailability of mercury Appl. Environ. Microb. 1997, 63, 4267-4271 (Pubitemid 27485749)
18. Graham, A. M.; Aiken, G. R.; Gilmour, C. C. Dissolved organic matter enhances microbial mercury methylation under sulfidic conditions Environ. Sci. Technol. 2012, 46, 2715-2723
19. Compeau, G. C.; Bartha, R. Sulfate-reducing bacteria-principal methylators of mercury in anoxic estuarine sediment Appl. Environ. Microb. 1985, 50, 498-502 (Pubitemid 15018782)
20. Gilmour, C. C.; Henry, E. A.; Mitchell, R. Sulfate stimulation of mercury methylation in freshwater sediments Environ. Sci. Technol. 1992, 26, 2281-2287 (Pubitemid 23376854)
21. Drott, A.; Lambertsson, L.; Bjorn, E.; Skyllberg, U. Importance of dissolved neutral mercury sulfides for methyl mercury production in contaminated sediments Environ. Sci. Technol. 2007, 41, 2270-2276 (Pubitemid 46595185)
22. Benoit, J.; Gilmour, C.; Mason, R.; Heyes, A. Sulfide controls on mercury speciation and bioavailability to methylating bacteria in sediment pore waters Environ. Sci. Technol. 1999, 33, 951-957 (Pubitemid 29140475)
23. Miller, C. L.; Mason, R. P.; Gilmour, C. C.; Heyes, A. Influence of dissolved organic matter on the complexation of mercury under sulfidic conditions Environ. Toxicol. Chem. 2007, 26, 624-633 (Pubitemid 46663262)
24. Deonarine, A.; Lau, B. L. T.; Aiken, G.; Ryan, J.; Hsu-Kim, H. Effects of humic substances on precipitation and aggregation of zinc sulfide nanoparticles Environ. Sci. Technol. 2011, 45, 3217-3223
25. Zhang, T.; Kim, B.; Levard, C.; Reinsch, B. C.; Lowry, G. V.; Deshusses, M. A.; Hsu-Kim, H. Methylation of mercury by bacteria exposed to dissolved, nanoparticulate, and microparticulate mercuric sulfides Environ. Sci. Technol. 2012, 46, 6950-6958
26. Weishaar, J. L.; Aiken, G. R.; Bergamaschi, B. A.; Fram, M. S.; Fujii, R.; Mopper, K. Evaluation of specific ultraviolet absorbance as an indicator of the chemical composition and reactivity of dissolved organic carbon Environ. Sci. Technol. 2003, 37, 4702-4708 (Pubitemid 37266389)
27. Hall, B. D.; Aiken, G. R.; Krabbenhoft, D. P.; Marvin-Dipasquale, M.; Swarzenski, C. M. Wetlands as principal zones of methylmercury production in southern Louisiana and the Gulf of Mexico region Environ. Pollut. 2008, 154, 124-134
28. Mitchell, C. P. J.; Gilmour, C. C. Methylmercury production in a Chesapeake Bay salt marsh J. Geophys. Res.-Biogeo. 2008, 113, G00C04
29. Gerbig, C. The effects of dissolved organic matter on mercury-sulfide interactions in aqueous systems, Ph.D. Dissertation, University of Colorado, 2011.
30. Dittman, J. A.; Shanley, J. B.; Driscoll, C. T.; Aiken, G. R.; Chalmers, A. T.; Towse, J. E.; Selvendiran, P. Mercury dynamics in relation to dissolved organic carbon concentration and quality during high flow events in three northeastern U.S. streams Water Resour. Res. 2010, 46, W07522
31. Aiken, G. R.; Gilmour, C. C.; Krabbenhoft, D. P.; Orem, W. Dissolved organic matter in the Florida Everglades: implications for ecosystem restoration Crit. Rev. Environ. Sci. Technol. 2011, 41, 217-248
32. Haaland, S.; Hongve, D.; Laudon, H.; Riise, G.; Vogt, R. D. Quantifying the drivers of the increasing colored organic matter in boreal surface waters Environ. Sci. Technol. 2010, 44, 2975-2980
33. SanClements, M. D.; Oelsner, G. P.; McKnight, D. M.; Stoddard, J. L.; Nelson, S. J. New insights into the source of decadal increases of dissolved organic matter in acid-sensitive lakes of the northeastern United States Environ. Sci. Technol. 2012, 46, 3212-3219
34. Thurman, E. M.; Malcolm, R. L. Preparative isolation of aquatic humic substances Environ. Sci. Technol. 1981, 15, 463-466 (Pubitemid 11104137)
35. Aiken, G.; McKnight, D.; Thorn, K. A.; Thurman, E. M. Isolation of hydrophilic organic-acids from water using nonionic macroporous resins Org. Geochem. 1992, 18, 567-573
36. Gilmour, C. C.; Tuttle, J. H.; Means, J. C. Anaerobic microbial methylation of inorganic tin in estuarine sediment slurries Microb. Ecol. 1987, 14, 233-242
37. Gilmour, C. C.; Elias, D. A.; Kucken, A. M.; Brown, S. D.; Palumbo, A. V.; Schadt, C. W.; Wall, J. D. Sulfate-reducing bacterium Desulfovibrio desulfuricans ND132 as a model for understanding bacterial mercury methylation Appl. Environ. Microb. 2011, 77, 3938-3951
38. Graham, A. M.; Bullock, A. L.; Maizel, A. C.; Elias, D. A.; Gilmour, C. C. A Detailed assessment of the kinetics of Hg-cell association, Hg methylation, and MeHg degradation in several Desulfovibrio species Appl. Environ. Microb. 2012, 78, 7337-7346
39. Brown, S. D.; Gilmour, C. C.; Kucken, A. M.; Wall, J. D.; Elias, D. A.; Brandt, C. C.; Podar, M.; Chertkov, O.; Held, B.; Bruce, D. C.; Detter, J. C.; Tapia, R.; Han, C. S.; Goodwin, L. A.; Cheng, J.-F.; Pitluck, S.; Woyke, T.; Mikhailova, N.; Ivanova, N. N.; Han, J.; Lucas, S.; Lapidus, A. L.; Land, M. L.; Hauser, L. J.; Palumbo, A. V. Genome sequence of the mercury-methylating strain Desulfovibrio desulfuricans ND132 J. Bacteriol. 2011, 193, 2078-2079
40. Schaefer, J. K.; Rocks, S. S.; Zheng, W.; Liang, L.; Gu, B.; Morel, F. M. M. Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 8714-8719
41. Clesceri, L. S.; Greenberg, A. E.; Eaton, A. D, Eds. Standard Methods for the Examination of Water and Wastewater; American Public Health Association: Washington, D.C., 2000.
42. Bradford, M. M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding Anal. Biochem. 1976, 72, 248-254
43. Hintelmann, H.; Ogrinc, N. Determination of stable mercury isotopes by ICP/MS and their application in environmental studies. In Biogeochemistry of Environmentally Important Trace Metals; Cai, Y.; Braids, C. O., Eds.; American Chemical Society: Washington, D.C., 2003; pp 321-338. (Pubitemid 135715782)
44. 198HgCl) Appl. Organomet. Chem. 2004, 18, 57-64
45. Schaefer, J. K.; Morel, F. M. M. High methylation rates of mercury bound to cysteine by Geobacter sulfurreducens Nat. Geosci. 2009, 2, 123-126
46. Helms, J. R.; Stubbins, A.; Ritchie, J. D.; Minor, E. C.; Kieber, D. J.; Mopper, K. Absorption spectral slopes and slope ratios as indicators of molecular weight, source, and photobleaching of chromophoric dissolved organic matter Limnol. Oceanogr. 2008, 53, 955-969 (Pubitemid 351821693)
47. Skyllberg, U. Competition among thiols and inorganic sulfides and polysulfides for Hg and MeHg in wetland soils and sediments under suboxic conditions: Illumination of controversies and implications for MeHg net production J. Geophys. Res.-Biogeo. 2008, 113, G00C03
48. Vairavamurthy, M.; Maletic, D.; Wang, S.; Manowitz, B.; Eglinton, T.; Lyons, T. Characterization of sulfur-containing functional groups in sedimentary humic substances by X-ray absorption near-edge structure spectroscopy Energy Fuels 1997, 11, 546-553 (Pubitemid 127559157)
49. Mason, R.; Reinfelder, J.; Morel, F. Uptake, toxicity, and trophic transfer of mercury in a coastal diatom Environ. Sci. Technol. 1996, 30, 1835-1845 (Pubitemid 26158565)
50. Benoit, J.; Gilmour, C.; Mason, R. Aspects of bioavailability of mercury for methylation in pure cultures of Desulfobulbus propionicus (1pr3) Appl. Environ. Microb. 2001, 67, 51-58 (Pubitemid 32044401)
51. Navrotsky, A.; Mazeina, L.; Majzlan, J. Size-driven structural and thermodynamic complexity in iron oxides Science 2008, 319, 1635-1638 (Pubitemid 351432493)
52. Gilmour, C.; Riedel, G.; Ederington, M.; Bell, J.; Benoit, J.; Gill, G.; Stordal, M. Methylmercury concentrations and production rates across a trophic gradient in the northern Everglades Biogeochemistry 1998, 40, 327-345 (Pubitemid 28107198)
53. Hollweg, T. A.; Gilmour, C. C.; Mason, R. P. Methylmercury production in sediments of Chesapeake Bay and the mid-Atlantic continental margin Mar. Chem. 2009, 114, 86-101
54. Hollweg, T. A.; Gilmour, C. C.; Mason, R. P. Mercury and methylmercury cycling in sediments of the mid-Atlantic continental shelf and slope Limnol. Oceanogr. 2010, 55, 2703-2722
55. Hammerschmidt, C.; Fitzgerald, W. Geochemical controls on the production and distribution of methylmercury in near-shore marine sediments Environ. Sci. Technol. 2004, 38, 1487-1495 (Pubitemid 38270693)
56. Hammerschmidt, C. R.; Fitzgerald, W. F.; Balcom, P. H.; Visscher, P. T. Organic matter and sulfide inhibit methylmercury production in sediments of New York/New Jersey Harbor Mar. Chem. 2008, 109, 165-182 (Pubitemid 351324028)
57. Benoit, J.; Gilmour, C.; Mason, R. The influence of sulfide on solid phase mercury bioavailability for methylation by pure cultures of Desulfobulbus propionicus (1pr3) Environ. Sci. Technol. 2001, 35, 127-132 (Pubitemid 32048414)
58. Marvin-DiPasquale, M.; Lutz, M. A.; Brigham, M. E.; Krabbenhoft, D. P.; Aiken, G. R.; Orem, W. H.; Hall, B. D. Mercury cycling in stream ecosystems. 2. Benthic methylmercury production and bed sediment-pore water partitioning Environ. Sci. Technol. 2009, 43, 2726-2732
59. Mitchell, C. P. J.; Branfireun, B. A.; Kolka, R. K. Spatial characteristics of net methylmercury production hot spots in peatlands Environ. Sci. Technol. 2008, 42, 1010-1016 (Pubitemid 351287152)