A coupled geochemical and biogeochemical approach to characterize the bioreactivity of dissolved organic matter from a headwater stream

Journal of Geophysical Research: Biogeosciences

Volumn 119, Issue 8, 2014, Pages 1520-1537

  Sleighter, Rachel L ^a   Cory, Rose M ^b   Kaplan, Louis A ^c   Abdulla, Hussain A N ^a   Hatcher, Patrick G ^a  

^a OLD DOMINION UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c STROUD WATER RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIODEGRADATION; BIOFILM; BIOGEOCHEMISTRY; BIOREACTOR; DISSOLVED ORGANIC MATTER; HEADWATER; MICROBIAL ACTIVITY; MOLECULAR ANALYSIS; STREAMWATER;

EID: 84924246190     PISSN: 21698953     EISSN: 21698961     Source Type: Journal    
DOI: 10.1002/2013JG002600     Document Type: Article

References (84)

1. Abdulla, H. A. N., R. L. Sleighter, and P. G. Hatcher (2013), Two dimensional correlation analysis of Fourier transform ion cyclotron resonance mass spectra of dissolved organic matter: A new graphical analysis of trends, Anal. Chem., 85(8), 3895-3902, doi:10.1021/ac303221j.
2. Aiken, G. R., D. M. McKnight, K. A. Thorn, and E. M. Thurman (1992), Isolation of hydrophilic organic acids from water using nonionic macroporous resins, Org. Geochem., 18(4), 567-573, doi:10.1016/0146-6380(92)90119-I.
3. Aufdenkampe, A. K., E. Mayorga, P. A. Raymond, J. M. Melack, S. C. Doney, S. R. Alin, R. E. Aalto, and K. Yoo (2011), Riverine coupling of biogeochemical cycles between land, oceans, and atmosphere, Front. Ecol. Environ., 9(1), 53-60, doi:10.1890/100014.
4. Balcarczyk, K. L., J. B. Jones Jr., R. Jaffé, and N. Maie (2009), Stream dissolved organic matter bioavailability and composition in watersheds underlain with discontinuous permafrost, Biogeochemistry, 94(3), 255-270, doi:10.1007/s10533-009-9324-x.
5. Battin, T. J., L. A. Kaplan, S. Findlay, C. S. Hopkinson, E. Marti, A. I. Packman, J. D. Newbold, and F. Sabater (2008), Biophysical controls on organic carbon fluxes in fluvial networks, Nat. Geosci., 1(2), 95-100, doi:10.1038/ngeo101.
6. Battin, T. J., S. Luyssaert, L. A. Kaplan, A. K. Aufdenkampe, A. Richter, and L. J. Tranvik (2009), The boundless carbon cycle, Nat. Geosci., 2(9), 598-600, doi:10.1038/ngeo618.
7. Benner, R. (2003), Molecular indicators of the bioavailability of dissolved organic matter, in Aquatic Ecosystems - Interactivity of Dissolved Organic Matter, edited by S. E. G. Findlay and R. L. Sinsabaugh, pp. 121-138, Academic Press, San Diego.
8. Carlson, C. A. (2002), Production and comsumption processes, in Biogeochemistry of Marine Dissolved Organic Matter, edited by D. A. Hansell and C. A. Carlson, pp. 91-151, Academic Press, San Diego.
9. Chin, Y.-P., G. R. Aiken, and K. M. Danielsen (1997), Binding of pyrene to aquatic and commercial humic substances: The role of molecular weight and aromaticity, Environ. Sci. Technol., 31(6), 1630-1635, doi:10.1021/es960404k.
10. Cleveland, C. C., J. C. Neff, A. R. Townsend, and E. Hood (2004), Composition, dynamics, and fate of leached dissolved organic matter in terrestrial ecosystems: Results from a decomposition experiment, Ecosystems, 7(3), 175-285, doi:10.1007/s10021-003-0236-7.
11. Coble, P. G. (1996), Characterization of marine and terrestrial DOM in seawater using excitation-emission matrix spectroscopy, Mar. Chem., 51(4), 325-346, doi:10.1016/0304-4203(95)00062-3.
12. Cole, J. J., and N. F. Caraco (2001), Carbon in catchments: Connecting terrestrial carbon losses with aquatic metabolism, Mar. Freshwater Res., 52(1), 101-110, doi:10.1071/MF00084.
13. Cole, J. J., et al. (2007), Plumbing the global carbon cycle: Integrating inland waters into the terrestrial carbon budget, Ecosystems, 10(1), 172-185, doi:10.1007/s10021-006-9013-8.
14. Cory, R. M., and L. A. Kaplan (2012), Biological lability of streamwater fluorescent dissolved organic matter, Limnol. Oceanogr., 57(5), 1347-1360, doi:10.4319/lo.2012.57.5.1347.
15. Cory, R. M., and L. A. Kaplan (2013), Erratum: Biological lability of streamwater fluorescent dissolved organic matter, Limnol. Oceanogr., 58(1), 428, doi:10.4319/lo.2013.58.1.0428.
16. Cory, R. M., and D. M. McKnight (2005), Fluorescence spectroscopy reveals ubiquitous presence of oxidized and reduced quinones in dissolved organic matter, Environ. Sci. Technol., 39(21), 8142-8149, doi:10.1021/es0506962.
17. Cory, R. M., D. M. McKnight, Y.-P. Chin, P. Miller, and C. L. Jaros (2007), Chemical characteristics of fulvic acids from Arctic surface waters: Microbial contributions and photochemical transformations, J. Geophys. Res., 112, G04S51, doi:10.1029/2006JG000343.
18. Cory, R. M., M. P. Miller, D. M. McKnight, J. J. Guerard, and P. L. Miller (2010a), Effect of instrument-specific response on the analysis of fulvic acid fluorescence spectra, Limnol. Oceanogr.: Methods, 8, 67-78, doi:10.4319/lom.2010.8.67.
19. Cory, R. M., K. McNeill, J. P. Cotner, A. Amado, J. M. Purcell, and A. G. Marshall (2010b), Singlet oxygen in the coupled photochemical and biochemical oxidation of dissolved organic matter, Environ. Sci. Technol., 44(10), 3683-3689.
20. 2 release from permafrost soil carbon in the Arctic, Proc. Natl. Acad. Sci. U.S.A., 110(9), 3429-3434, doi:10.1073/pnas.1214104110.
21. Cowie, G. L., and J. I. Hedges (1992), Sources and reactivities of amino acids in a coastal marine environment, Limnol. Oceanogr., 37(4), 703-724.
22. Cummins, K. W., J. J. Klug, R. G. Wetzel, R. C. Petersen, K. F. Suberkropp, B. A. Manny, J. C. Wuycheck, and F. O. Howard (1972), Organic enrichment with leaf leachate in experimental lotic ecosystems, BioScience, 22(12), 719-722, stable URL: http://www.jstor.org/stable/1296289.
23. Cuss, C. W., and C. Guéguen (2012), Impacts of microbial activity on the optical and copper-binding properties of leaf-litter leachate, Front. Microbiol., 3(166), 1-10, doi:10.3389/fmicb.2012.00166.
24. del Vecchio, R., and N. V. Blough (2004), On the origin of the optical properties of humic substances, Environ. Sci. Technol., 38(14), 3885-3891, doi:10.1021/es049912h.
25. Dittmar, T., B. Koch, N. Hertkorn, and G. Kattner (2008), A simple and efficient method for the solid phase extraction of dissolved organic matter (SPE-DOM) from seawater, Limnol. Oceanogr.: Methods, 6, 230-235, doi:10.4319/lom.2008.6.230.
26. Fellman, J. B., D. V. D'Amore, E. Hood, and R. D. Boone (2008), Fluorescence characteristics and biodegradability of dissolved organic matter in forest and wetland soils from coastal temperate watersheds in southeast Alaska, Biogeochemistry, 88(2), 169-184, doi:10.1007/s10533-008-9203-x.
27. Fellman, J. B., E. Hood, R. T. Edwards, and D. V. D'Amore (2009a), Changes in the concentration, biodegradability, and fluorescent properties of dissolved organic matter during storm flows in coastal temperate watersheds, J. Geophys. Res., 114, G01021, doi:10.1029/2008JG000790.
28. Fellman, J. B., E. Hood, D. V. D'Amore, R. T. Edwards, and D. White (2009b), Seasonal changes in the chemical quality and biodegradability of dissolved organic matter exported from soils to streams in coastal temperate rainforest watersheds, Biogeochemistry, 95(2-3), 277-293, doi:10.1007/s10533-009-9336-6.
29. Fellman, J. B., R. G. M. Spencer, P. J. Hernes, R. T. Edwards, D. V. D'Amore, and E. Hood (2010), The impact of glacier runoff on the biodegradability and biochemical composition of terrigenous dissolved organic matter in near-shore marine ecosystems, Mar. Chem., 121(1-4), 112-122, doi:10.1016/j.marchem.2010.03.009.
30. 13C] tetramethylammonium hydroxide thermochemolysis GC-MS, Environ. Sci. Technol., 39(6), 1479-1491, doi:10.1021/es0494959.
31. Gonsior, M., B. M. Peake, W. T. Cooper, D. Podgorski, J. D'Andrilli, and W. J. Cooper (2009), Photochemically induced changes in dissolved organic matter identified by ultrahigh resolution Fourier transform ion cyclotron resonance mass spectrometry, Environ. Sci. Technol., 43(3), 698-703, doi:10.1021/es8022804.
32. Gonsior, M., B. M. Peake, W. T. Cooper, D. C. Podgorski, J. D'Andrilli, T. Dittmar, and W. J. Cooper (2011), Characterization of dissolved organic matter across the Subtropical Convergence off the South Island, New Zealand, Mar. Chem., 123(1-4), 99-110, doi:10.1016/j.marchem.2010.10.004.
33. Grace, J., and Y. Malhi (2002), Global change: Carbon dioxide goes with the flow, Nature, 416(6881), 594, doi:10.1038/416594b.
34. Guillemette, F., and P. A. del Giorgio (2011), Reconstructing the various facets of dissolved organic carbon bioavailability in freshwater ecosystems, Limnol. Oceanogr., 56(2), 734-748, doi:10.4319/lo.2011.56.2.0734.
35. Helms, J. R., A. Stubbins, J. D. Ritchie, E. C. Minor, D. J. Kieber, and K. Mopper (2008), Absorption spectral slopes and slope ratios as indicators of molecular weight, source, and photobleaching of chromophoric dissolved organic matter, Limnol. Oceanogr., 53(3), 955-969, doi:10.4319/lo.2008.53.3.0955.
36. Hernes, P. J., B. A. Bergamaschi, R. S. Eckard, and R. G. M. Spencer (2009), Fluorescence-based proxies for lignin in freshwater dissolved organic matter, J. Geophys. Res., 114, G00F03, doi:10.1029/2009JG000938.
37. Herzsprung, P., W. von Tümpling, N. Hertkorn, M. Harir, O. Büttner, J. Bravidor, K. Friese, and P. Schmitt-Kopplin (2012), Variations of DOM quality in inflows of a drinking water reservoir: Linking of van Krevelen diagrams with EEMF spectra by rank correlation, Environ. Sci. Technol., 46(10), 5511-5518, doi:10.1021/es300345c.
38. Hockaday, W. C., J. M. Purcell, A. G. Marshall, J. A. Baldock, and P. G. Hatcher (2009), Electrospray and photoionization mass spectrometry for the characterization of organic matter in natural waters: A qualitative assessment, Limnol. Oceanogr.: Methods, 7, 81-95, doi:10.4319/lom.2009.7.81.
39. Hood, E., J. Fellman, R. G. M. Spencer, P. J. Hernes, R. Edwards, D. D'Amore, and D. Scott (2009), Glaciers as a source of ancient and labile organic matter to the marine environment, Nature, 462(7276), 1044-1047, doi:10.1038/nature08580.
40. Hopkinson, C. S., et al. (1998), Terrestrial inputs of organic matter to coastal ecosystems: An intercomparison of chemical characteristics and bioavailability, Biogeochemistry, 43(3), 211-234, doi:10.1023/A:1006016030299.
41. Kaplan, L. A., and J. D. Newbold (1993), Biogeochemistry of dissolved organic carbon entering streams, in Aquatic Microbiology- An Ecological Approach, edited by T. E. Ford, pp. 139-165, Blackwell Scientific, Cambridge, U. K.
42. Kaplan, L. A., and J. D. Newbold (1995), Measurement of streamwater biodegradable dissolved organic carbon with a plug-flow bioreactor, Water Res., 29(12), 2696-2706, doi:10.1016/0043-1354(95)00135-8.
43. Kaplan, L. A., and J. D. Newbold (2003), The role of monomers in stream ecosystem metabolism, in Aquatic Ecosystems - Interactivity of Dissolved Organic Matter, edited by S. E. G. Findlay and R. L. Sinsabaugh, pp. 97-119, Academic Press, San Diego.
44. Kaplan, L. A., T. N. Wiegner, J. D. Newbold, P. H. Ostrom, and H. Gandhi (2008), Untangling the complex issue of dissolved organic carbon uptake: A stable isotope approach, Freshwater Biol., 53(5), 855-864, doi:10.1111/j.1365-2427.2007.01941.x.
45. Kim, S., L. A. Kaplan, and P. G. Hatcher (2006), Biodegradable dissolved organic matter in a temperate and a tropical stream determined from ultra-high resolution mass spectrometry, Limnol. Oceanogr., 51(2), 1054-1063, doi:10.4319/lo.2006.51.2.1054.
46. Kirchman, D. L. (2003), The contribution of monomers and other low molecular weight compounds to the flux of dissolved organic matter in aquatic ecosystems, in Aquatic Ecosystems - Interactivity of Dissolved Organic Matter, edited by S. E. G. Findlay and R. L. Sinsabaugh, pp. 218-241, Academic Press, San Diego.
47. Koch, B. P., and T. Dittmar (2006), From mass to structure: An aromaticity index for high-resolution mass data of natural organic matter, Rapid Commun. Mass Spectrom., 20(5), 926-932, doi:10.1002/rcm.2386.
48. Koch, B. P., M. Witt, R. Engbrodt, T. Dittmar, and G. Kattner (2005), Molecular formulae of marine and terrigenous dissolved organic matter detected by electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry, Geochim. Cosmochim. Acta, 69(13), 3299-3308, doi:10.1016/j.gca.2005.02.027.
49. Koehler, B., E. von Wachenfeldt, D. Kothawala, and L. J. Tranvik (2012), Reactivity continuum of dissolved organic carbon decomposition in lake water, J. Geophys. Res., 117, G01024, doi:10.1029/2011JG001793.
50. Mann, P. J., A. Davydova, N. Zimov, R. G. M. Spencer, S. Davydov, E. Bulygina, S. Zimov, and R. M. Holmes (2012), Controls on the composition and lability of dissolved organic matter in Siberia's Kolyma River basin, J. Geophys. Res., 117, G01028, doi:10.1029/2011JG001798.
51. Marshall, A. G., C. L. Hendrickson, and G. S. Jackson (1998), Fourier transform ion cyclotron resonance mass spectrometry: A primer, Mass Spectrom. Rev., 17(1), 1-35, doi:10.1002/(SICI)1098-2787(1998)17:1〈1::AID-MAS1〉3.0.CO;2-K.
52. Mayer, L. M., R. G. Keil, S. A. Macko, S. B. Joye, K. C. Ruttenberg, and R. C. Aller (1998), Importance of suspended participates in riverine delivery of bioavailable nitrogen to coastal zones, Global Biogeochem. Cycles, 12(4), 573-579, doi:10.1029/98GB02267.
53. McKnight, D. M., E. W. Boyer, P. K. Westerhoff, P. T. Doran, T. Kulbe, and D. T. Andersen (2001), Spectro fluorometric characterization of dissolved organic matter for indication of precursor organic material and aromaticity, Limnol. Oceanogr., 46(1), 38-48, doi:10.4319/lo.2001.46.1.0038.
54. McLaughlin, C., and L. A. Kaplan (2013), Biological lability of dissolved organic carbon in stream water and contributing terrestrial sources, Freshwater Sci., 32(4), 1219-1230, doi:10.1899/12-202.1.
55. Michaelson, G. J., C. L. Ping, G. W. Kling, and J. E. Hobbie (1998), The character and bioactivity of dissolved organic matter at thaw and in the spring runoff waters of the arctic tundra North Slope, Alaska, J. Geophys. Res., 103, 28,939-28,946, doi:10.1029/98JD02650.
56. Murphy, K. R., C. A. Stedmon, T. D. Waite, and G. M. Ruiz (2008), Distinguishing between terrestrial and autochthonous organic matter sources in marine environments using fluorescence spectroscopy, Mar. Chem., 108(1-2), 40-58, doi:10.1016/j.marchem.2007.10.003.
57. Newbold, J. D., T. L. Bott, L. A. Kaplan, B. W. Sweeney, and R. L. Vannote (1997), Organic matter dynamics in White Clay Creek, Pennsylvania, USA, J. N. Am. Benthol. Soc., 16(1), 46-50, stable URL: http://www.jstor.org/stable/1468231.
58. Ohno, T., Z. He, R. L. Sleighter, C. W. Honeycutt, and P. G. Hatcher (2010), Ultrahigh resolution mass spectrometry and indicator species analysis to identify marker components of soil- and plant biomass-derived organic matter fractions, Environ. Sci. Technol., 44(22), 8594-8600, doi:10.1021/es101089t.
59. Reemtsma, T. (2009), Determination of molecular formulas of natural organic matter molecules by (ultra-) high-resolution mass spectrometry: Status and needs, J. Chromatogr. A, 1216(18), 3687-3701, doi:10.1016/j.chroma.2009.02.033.
60. 2, Nature, 416(6881), 617-620, doi:10.1038/416617a.
61. 2, Science, 305(5682), 367-371, doi:10.1126/science.1097403.
62. Sleighter, R. L., and P. G. Hatcher (2007), The application of electrospray ionization coupled to ultrahigh resolution mass spectrometry for the molecular characterization of natural organic matter, J. Mass Spectrom., 42(5), 559-574, doi:10.1002/jms.1221.
63. Sleighter, R. L., and P. G. Hatcher (2008), Molecular characterization of dissolved organic matter (DOM) along a river to ocean transect of the lower Chesapeake Bay by ultrahigh resolution electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry, Mar. Chem., 110(3-4), 140-152, doi:10.1016/j.marchem.2008.04.008.
64. Sleighter, R. L., and P. G. Hatcher (2011), Fourier transform mass spectrometry for the molecular level characterization of natural organic matter: Instrument capabilities, applications, and limitations, in Fourier Transforms - Approach to Scientific Principles, edited by G. Nikolic, pp. 295-320, InTech, Vienna, stable URL: http://www.intechopen.com/articles/show/title/fourier-transform-mass-spectrometry-for-the-molecular-level-characterization-of-natural-organic-matt.
65. Sleighter, R. L., G. A. McKee, Z. Liu, and P. G. Hatcher (2008), Naturally present fatty acids as internal calibrants for Fourier transform mass spectra of dissolved organic matter, Limnol. Oceanogr.: Methods, 6, 246-253, doi:10.4319/lom.2008.6.246.
66. Sleighter, R. L., G. A. McKee, and P. G. Hatcher (2009), Direct Fourier transform mass spectral analysis of natural waters with low dissolved organic matter, Org. Geochem., 40(1), 119-125, doi:10.1016/j.orggeochem.2008.09.012.
67. Sleighter, R. L., Z. Liu, J. Xue, and P. G. Hatcher (2010), Multivariate statistical approaches for the characterization of dissolved organic matter analyzed by ultrahigh resolution mass spectrometry, Environ. Sci. Technol., 44(19), 7576-7582, doi:10.1021/es1002204.
68. Sleighter, R. L., H. Chen, A. S. Wozniak, A. S. Willoughby, P. Caricasole, and P. G. Hatcher (2012), Establishing a measure of reproducibility of ultrahigh-resolution mass spectra for complex mixtures of natural organic matter, Anal. Chem., 84(21), 9184-9191, doi:10.1021/ac3018026.
69. Stedmon, C. A., and S. Markager (2005), Tracing the production and degradation of autochthonous fractions of dissolved organic matter by fluorescence analysis, Limnol. Oceanogr., 50(5), 1415-1426, doi:10.4319/lo.2005.50.5.1415.
70. Stenson, A. C., W. M. Landing, A. G. Marshall, and W. T. Cooper (2002), Ionization and fragmentation of humic substances in electrospray ionization Fourier transform-ion cyclotron resonance mass spectrometry, Anal. Chem., 74(17), 4397-4409, doi:10.1021/ac020019f.
71. Stenson, A. C., A. G. Marshall, and W. T. Cooper (2003), Exact masses and chemical formulas of individual Suwannee River fulvic acids from ultrahigh resolution electrospray ionization Fourier transform ion cyclotron resonance mass spectra, Anal. Chem., 75(6), 1275-1284, doi:10.1021/ac026106p.
72. Stubbins, A., R. G. M. Spencer, H. Chen, P. G. Hatcher, K. Mopper, P. J. Hernes, V. L. Mwamba, A. M. Mangangu, J. N. Wabakanghanzi, and J. Six (2010), Illuminated darkness: Molecular signatures of Congo River dissolved organic matter and its photochemical alteration as revealed by ultrahigh precision mass spectrometry, Limnol. Oceanogr., 55(4), 1467-1477, doi:10.4319/lo.2010.55.3.1467.
73. Stubbins, A., et al. (2012), Anthropogenic aerosols as a source of ancient dissolved organic matter in glaciers, Nat. Geosci., 5(3), 198-201, doi:10.1038/ngeo1403.
74. Stubbins, A., P. A. del Giorgio, M. Berggren, J. F. Lapierre, and T. Dittmar (2013), What's in an EEM? Molecular signatures associated with dissolved organic fluorophores, paper presented at the Association for the Sciences of Limnology and Oceanography (ASLO) 2013 Aquatic Sciences Meeting, New Orleans, La.
75. Sweeney, B. W. (1993), Effects of streamside vegetation on macroinvertebrate communities of White Clay Creek, Proc. Acad. Nat. Sci. Philadelphia, 144, 291-340, stable URL: http://www.jstor.org/stable/4065013.
76. Tranvik, L. J., and S. Bertilsson (2001), Contrasting effects of solar UV radiation on dissolved organic sources for bacterial growth, Ecol. Lett., 4(5), 458-463, doi:10.1046/j.1461-0248.2001.00245.x.
77. Tranvik, L. J., et al. (2009), Lakes and reservoirs as regulators of carbon cycling and climate, Limnol. Oceanogr., 54(6), 2298-2314, doi:10.4319/lo.2009.54.6-part-2.2298.
78. Vähätalo, A. V., H. Aarnos, and S. Mäntyniemi (2010), Biodegradability continuum and biodegradation kinetics of natural organic matter described by the beta distribution, Biogeochemistry, 100(1-3), 227-240, doi:10.1007/s10533-010-9419-4.
79. Volk, C. J., C. B. Volk, and L. A. Kaplan (1997), Chemical composition of biodegradable dissolved organic matter in streamwater, Limnol. Oceanogr., 42 (1), 39-44, stable URL: http://www.jstor.org/stable/2838860.
80. Ward, N. D., R. G. Keil, P. M. Medeiros, D. C. Brito, A. C. Cunha, T. Dittmar, P. L. Yager, A. V. Krusche, and J. E. Richey (2013), Degradation of terrestrially derived macromolecules in the Amazon River, Nat. Geosci., 6(7), 530-533, doi:10.1038/ngeo1817.
81. Westrich, J. T., and R. A. Berner (1984), The role of sedimentary organic matter in bacterial sulfate reduction: The G model tested, Limnol. Oceanogr., 29(2), 236-249.
82. Wetzel, R. G. (2003), Dissolved organic carbon: Detrital energetics, metabolic regulators, and drivers of ecosystem stability of aquatic ecosystems, in Aquatic Ecosystems-Interactivity of Dissolved Organic Matter, edited by S. E. G. Findlay and R. L. Sinsabaugh, pp. 455-477, Academic Press, San Diego.
83. Wickland, K. P., J. C. Neff, and G. R. Aiken (2007), Dissolved organic carbon in Alaskan boreal forest: Sources, chemical characteristics, and biodegradability, Ecosystems, 10(8), 1323-1340, doi:10.1007/s10021-007-9101-4.
84. Yamashita, Y., and E. Tanoue (2003), Chemical characterization of protein-like fluorophores in DOM in relation to aromatic amino acids, Mar. Chem., 82 (3-4), 255-271, doi:10.1016/S0304-4203(03)00073-2.