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Measuring the influence of environmental conditions on dissolved organic matter biodegradability and optical properties: a combined field and laboratory study

Abstract

Fluorescence spectroscopy is a common tool to assess optical dissolved organic matter (DOM) and a number of characteristics, including DOM biodegradability, have been inferred from these analyses. However, recent findings on soil and DOM dynamics emphasize the importance of ecosystem-scale factors, such as physical separation of substrate from soil microbial communities and soil physiochemical cycles driving DOM stability. We apply this principle to soil derived DOM and hypothesize that optical properties can only supply information on biodegradability when evaluated in the larger ecosystem because substrate composition and the activity/abundance of the microbial community ultimately drive DOM degradation. To evaluate biodegradability in this context, we assessed aqueous soil extracts for water extractable organic carbon (WEOC) content, biodegradability, microbial biomass and DOM characteristics using fluorescence spectroscopy across a range of environmental conditions (covariant with season and land use) in northern Vermont, USA. Our results indicate that changes in environmental conditions affect composition, quantity, and biodegradability of DOM. WEOC concentrations were highest in the fall and lowest in the summer, while no significant differences were found between land covers; however, DOM biodegradability was significantly higher in the agricultural site across seasons. Despite a shift in utilized substrate from less aromatic DOM in summer to more aromatic DOM in winter, biodegradability was similar for all seasons. The only exception was cold temperature incubations where microbial activity was depressed, and processing was slowed. These results provide examples on how fluorescence based metrics can be combined with context relevant environmental parameters to evaluate bioavailability in the context of the larger ecosystem.

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References

  1. Andrews D, Lin H, Zhu Q, Jin L, Brantley S (2011) Hot spots and hot moments of dissolved organic carbon export and soil organic carbon storage in the shale hills catchment. Vadose Zone J 10:943

    Google Scholar 

  2. Blume E, Gray M, Reichert JM, Moorman T, Konopka A, Turco R (2002) Surface and subsurface microbial biomass, community structure and metabolic activity as a function of soil depth and season. Appl Soil Ecol 20:171–181

    Google Scholar 

  3. Bond-Lamberty B, Smith AP, Bailey V (2016) Temperature and moisture effects on greenhouse gas emissions from deep active-layer boreal soils. Biogeosciences 13(24):6669–6681

    Google Scholar 

  4. Bro R (1997) PARAFAC. Tutorial and applications. Chemom Intell Lab Syst 38(2):149–171

    Google Scholar 

  5. Cincotta MM, Perdrial JN, Shavitz A, Libenson A, Landsman-Gerjoi M, Perdrial N, Armfield J, Adler T, Shanley JB (2019) Soil aggregates as a source of dissolved organic carbon to streams: an experimental study on the effect of solution chemistry on water extractable carbon. Front Environ Sci 7:172

    Google Scholar 

  6. Cole JJ, Prairie YT, Caraco NF, McDowell WH, Tranvik LJ, Striegl RG, Duarte CM, Kortelainen P, Downing JA, Middelburg JJ, Melack J (2007) Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10(1):172–185

    Google Scholar 

  7. Contosta AR, Frey SD, Cooper AB (2011) Seasonal dynamics of soil respiration and N mineralization in chronically warmed and fertilized soils. Ecosphere 2(3):art36

    Google Scholar 

  8. Cory RM, McKnight DM (2005) Fluorescence spectroscopy reveals ubiquitous presence of oxidized and reduced quinones in dissolved organic matter. Environ Sci Technol 39(21):8142–8149

    Google Scholar 

  9. Cory R, Boyer E, McKnight D (2011) Spectral methods to advance understanding of dissolved organic carbon dynamics in forested catchments. For Hydrol Biogeochem. https://doi.org/10.1007/978-94-007-1363-5_6

    Article  Google Scholar 

  10. D’Andrilli J, Junker JR, Smith HJ, Scholl EA, Foreman CM (2019) DOM composition alters ecosystem function during microbial processing of isolated sources. Biogeochemistry 142(2):281–298

    Google Scholar 

  11. Estop-Aragonés C, Cooper MDA, Fisher JP, Thierry A, Garnett MH, Charman DJ, Murton JB, Phoenix GK, Treharne R, Sanderson NK, Burn CR, Kokelj SV, Wolfe SA, Lewkowicz AG, Williams M, Hartley IP (2018) Limited release of previously-frozen C and increased new peat formation after thaw in permafrost peatlands. Soil Biol Biochem 118:115–129

    Google Scholar 

  12. Fellman J, D’Amore D, Hood E, Boone R (2008) Fluorescence characteristics and biodegradability of dissolved organic matter in forest and wetland soils from coastal temperate watersheds in Southeast Alaska. Biogeochemistry 88:169–184

    Google Scholar 

  13. Fellman J, Hood E, Edwards RT, D’Amore D (2009a) Changes in the concentration, biodegradability, and fluorescent properties of dissolved organic matter during stormflows in coastal temperate watersheds. J Geophys Res: Biogeosci. https://doi.org/10.1029/2008JG000790

    Article  Google Scholar 

  14. Fellman J, Miller M, Cory R, D’Amore D, White D (2009b) Characterizing dissolved organic matter using PARAFAC modeling of fluorescence spectroscopy: a comparison of two models. Environ Sci Technol 43:6228–6234

    Google Scholar 

  15. Fierer N (2003) Stress ecology and the dynamics of microbial communities and processes in soil. University of California, Berkeley, p 226

    Google Scholar 

  16. Hansen AM, Kraus TEC, Pellerin BA, Fleck JA, Downing BD, Bergamaschi BA (2016) Optical properties of dissolved organic matter (DOM): effects of biological and photolytic degradation. Limnol Oceanogr 61(3):1015–1032

    Google Scholar 

  17. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (2000) Competition between roots and soil micro-organisms for nutrients from nitrogen-rich patches of varying complexity. J Ecol 88(1):150–164

    Google Scholar 

  18. Hongve D, Van Hees PAW, Lundström SU (2008) Dissolved components in precipitation water percolated through forest litter. Eur J Soil Sci 51:667–677

    Google Scholar 

  19. Inamdar S, Finger N, Singh S, Mitchell M, Levia D, Bais H, Scott D, McHale P (2012) Dissolved organic matter (DOM) concentration and quality in a forested mid-Atlantic watershed, USA. Biogeochemistry 108(1):55–76

    Google Scholar 

  20. IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  21. IPCC (2014) Climate change 2014: synthesis report. In: Core Writing Team, Pachauri RK, Meyer LA (eds) Contribution of working groups I II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC, Geneva

    Google Scholar 

  22. Ishii SKL, Boyer TH (2012) Behavior of reoccurring PARAFAC components in fluorescent dissolved organic matter in natural and engineered systems: a critical review. Environ Sci Technol 46(4):2006–2017

    Google Scholar 

  23. Johnson M, Couto E, Abdo M, Lehmann J (2011) Fluorescence index as an indicator of dissolved organic carbon quality in hydrologic flowpaths of forested tropical watersheds. Biogeochemistry 105:149–157

    Google Scholar 

  24. Kalbitz K, Schmerwitz J, Schwesig D, Matzner E (2003) Biodegradation of soil-derived dissolved organic matter as related to its properties. Geoderma 113(3):273–291

    Google Scholar 

  25. Khamis K, Bradley C, Hannah DM (2018) Understanding dissolved organic matter dynamics in urban catchments: insights from in situ fluorescence sensor technology. Wiley Interdiscip Rev: Water 5(1):e1259

    Google Scholar 

  26. Kim E-A, Lee HK, Choi JH (2017) Effects of a controlled freeze-thaw event on dissolved and colloidal soil organic matter. Environ Sci Pollut Res 24(2):1338–1346

    Google Scholar 

  27. Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198(3):656–669

    Google Scholar 

  28. Lai L, Zhao X, Jiang L, Wang Y, Luo L, Zheng Y, Chen X, Rimmington GM (2012) Soil respiration in different agricultural and natural ecosystems in an arid region. PLoS ONE 7(10):e48011

    Google Scholar 

  29. Lambert T, Bouillon S, Darchambeau F, Morana C, Roland FAE, Descy J-P, Borges AV (2017) Effects of human land use on the terrestrial and aquatic sources of fluvial organic matter in a temperate river basin (The Meuse River, Belgium). Biogeochemistry 136(2):191–211

    Google Scholar 

  30. LeCleir GR, Saxton MA, Wilhelm SW, Bullerjahn GS, McKay RM, Twiss MR, Bourbonniere RA (2014) Seasonal changes in microbial community structure and activity imply winter production is linked to summer hypoxia in a large lake. FEMS Microbiol Ecol 87(2):475–485

    Google Scholar 

  31. Marín-Spiotta E, Gruley K, Crawford J, Atkinson E, Miesel J, Greene S, Cardona-Correa C, Spencer R (2014) Paradigm shifts in soil organic matter research affect interpretations of aquatic carbon cycling: transcending disciplinary and ecosystem boundaries. Int J 117(2–3):279–297

    Google Scholar 

  32. Marschner B, Kalbitz K (2003) Controls of bioavailability and biodegradability of dissolved organic matter in soils. Geoderma 113(3):211–235

    Google Scholar 

  33. Matzner E, Borken W (2008) Do freeze-thaw events enhance C and N losses from soils of different ecosystems? A review. Eur J Soil Sci 59(2):274–284

    Google Scholar 

  34. McDowell W, Zsolnay A, Aitkenhead-Peterson J, Gregorich E, Jones D, Jödemann D, Kalbitz K, Marschner B, Schwesig D (2006) A comparison of methods to determine the biodegradable dissolved organic carbon from different terrestrial sources. Soil Biol Biochem 38(7):1933–1942

    Google Scholar 

  35. McKnight DM, Boyer EW, Westerhoff PK, Doran PT, Kulbe T, Andersen DT (2001) Spectrofluorometric characterization of dissolved organic matter for indication of precursor organic material and aromaticity. Limnol Oceanogr 46(1):38–48

    Google Scholar 

  36. Meyer JL, Wallace JB, Eggert SL (1998) Leaf litter as a source of dissolved organic carbon in streams. Ecosystems 1(3):240–249

    Google Scholar 

  37. Miller MP, McKnight DM (2010) Comparison of seasonal changes in fluorescent dissolved organic matter among aquatic lake and stream sites in the Green Lakes Valley. J Geophys Res: Biogeosci. https://doi.org/10.1029/2009JG000985

    Article  Google Scholar 

  38. Murphy KR, Stedmon CA, Graeber D, Bro R (2013) Fluorescence spectroscopy and multi-way techniques. PARAFAC. Anal Methods 5(23):6557–6566

    Google Scholar 

  39. Ohno T (2002) Fluorescence inner-filtering correction for determining the humification index of dissolved organic matter. Environ Sci Technol 36(4):742–746

    Google Scholar 

  40. Osterman M (2018) Carbon dioxide in agricultural streams: magnitude and patterns of an understudied atmospheric carbon source. In: UPTEC W. p 49

  41. Panneer Selvam B, Lapierre J-F, Guillemette F, Voigt C, Lamprecht RE, Biasi C, Christensen TR, Martikainen PJ, Berggren M (2017) Degradation potentials of dissolved organic carbon (DOC) from thawed permafrost peat. Sci Rep 7:45811

    Google Scholar 

  42. Parr TB, Cronan CS, Ohno T, Findlay SEG, Smith SMC, Simon KS (2015) Urbanization changes the composition and bioavailability of dissolved organic matter in headwater streams. Limnol Oceanogr 60(3):885–900

    Google Scholar 

  43. Perdrial JN, Perdrial N, Harpold A, Gao X, Gabor R, LaSharr K, Chorover J (2012a) Impacts of sampling dissolved organic matter with passive capillary wicks versus aqueous soil extraction. Soil Sci Soc Am J 76(6):2019–2030

    Google Scholar 

  44. Perdrial JN, Perdrial N, Harpold A, Gao X, LaSharr KM, Chorover J (2012b) Impacts of sampling dissolved organic matter with passive capillary wicks versus aqueous soil extraction. Soil Sci Soc Am J 76:2019–2030

    Google Scholar 

  45. Phillips CL, Nickerson N (2015) Soil respiration. In: Reference Module in earth systems and environmental sciences. Elsevier

  46. Qualls RG, Haines BL (1992) Biodegradability of dissolved organic matter in forest throughfall, soil solution, and stream water. Soil Sci Soc Am J 56(2):578–586

    Google Scholar 

  47. Ross DS (2019) Soil classification for BREE sites. In. Plant and soil science. University of Vermont, Vermont

  48. Schmidt MW, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kogel-Knabner I, Lehmann J, Manning DA, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478(7367):49–56

    Google Scholar 

  49. Setia R, Verma SL, Marschner P (2012) Measuring microbial biomass carbon by direct extraction—comparison with chloroform fumigation-extraction. Eur J Soil Biol 53:103–106

    Google Scholar 

  50. Singh S, Inamdar S, Mitchell M, McHale P (2013) Seasonal pattern of dissolved organic matter (DOM) in watershed sources: influence of hydrologic flow paths and autumn leaf fall. Biogeochemistry 118(1–3):321–337

    Google Scholar 

  51. Soil Survey Staff (2019) National Resources Conservation Service United States Department of Agriculture (Web Soil Survey)

  52. Sparks DL (2003) Environmental soil chemistry, 2nd edn. Academic Press, Burlington, pp 1–352

    Google Scholar 

  53. Stedmon C, Markager S, Bro R (2003) Tracing dissolved organic matter in aquatic environments using a new approach to fluorescence spectroscopy. Mar Chem 82(3–4):239–254

    Google Scholar 

  54. Stielstra CM, Lohse KA, Chorover J, McIntosh JC, Barron-Gafford GA, Perdrial JN, Litvak M, Barnard HR, Brooks PD (2015) Climatic and landscape influences on soil moisture are primary determinants of soil carbon fluxes in seasonally snow-covered forest ecosystems. Biogeochemistry 123(3):447–465

    Google Scholar 

  55. Strid A, Lee BS, Lajtha K (2016) Homogenization of detrital leachate in an old-growth coniferous forest, OR: DOC fluorescence signatures in soils undergoing long-term litter manipulations. Plant Soil 408(1):133–148

    Google Scholar 

  56. Swift RS (1996) Organic matter characterization. In: Sparks DL, Page AL, Helmke PA et al (eds) Methods of soil analysis, Part 3 chemical methods. Soil Science Society of America and American Society of Agronomy, Madison, Wis, USA, pp 1011–1069

    Google Scholar 

  57. Tan KH (2005) Soil sampling, preparation, and analysis. CRC Press, Boca Raton

    Google Scholar 

  58. Tate KR, Ross DJ, Feltham CW (1988) A direct extraction method to estimate soil microbial C: effects of experimental variables and some different calibration procedures. Soil Biol Biochem 20(3):329–335

    Google Scholar 

  59. Van Leeuwen J, Djukic I, Bloem J, Sandén T, Hemerik L, Ruiter P, Lair JG (2017) Effects of land use on soil microbial biomass, activity and community structure at different soil depths in the Danube floodplain. Eur J Soil Biol 79:14–20

    Google Scholar 

  60. Vaughan MCH, Bowden WB, Shanley JB, Vermilyea A, Sleeper R, Gold AJ, Pradhanang SM, Inamdar SP, Levia DF, Andres AS, Birgand F, Schroth AW (2017) High-frequency dissolved organic carbon and nitrate measurements reveal differences in storm hysteresis and loading in relation to land cover and seasonality. Water Resour Res 53(7):5345–5363

    Google Scholar 

  61. Wei H, Guenet B, Vicca S, Nunan N, Asard H, AbdElgawad H, Shen W, Janssens IA (2014) High clay content accelerates the decomposition of fresh organic matter in artificial soils. Soil Biol Biochem 77:100–108

    Google Scholar 

  62. Weishaar JL, Aiken GR, Bergamaschi BA, Fram MS, Fujii R, Mopper K (2003) Evaluation of specific ultraviolet absorbance as an indicator of the chemical composition and reactivity of dissolved organic carbon. Environ Sci Technol 37(20):4702–4708

    Google Scholar 

  63. Whittinghill KA, Finlay JC, Hobbie SE (2014) Bioavailability of dissolved organic carbon across a hillslope chronosequence in the Kuparuk River region, Alaska. Soil Biol Biochem 79:25–33

    Google Scholar 

  64. Wiegner TN, Tubal RL (2010) Comparison of dissolved organic carbon bioavailability from native and invasive vegetation along a Hawaiian River. Pac Sci 64:545–555

    Google Scholar 

  65. Wipf S, Sommerkorn M, Stutter MI, Wubs ERJ, van der Wal R (2015) Snow cover, freeze-thaw, and the retention of nutrients in an oceanic mountain ecosystem. Ecosphere 6(10):art207

    Google Scholar 

  66. Wong JCY, Williams DD (2010) Sources and seasonal patterns of dissolved organic matter (DOM) in the hyporheic zone. Hydrobiologia 647(1):99–111

    Google Scholar 

  67. Wymore A, Compson Z, McDowell W, Potter J, Hungate B, Whitham GT, Marks CJ (2015) Leaf-litter leachate is distinct in optical properties and bioavailability to stream heterotrophs. Freshw Sci 34(3):857–866

    Google Scholar 

  68. Xie W, Zhang S, Ruan L, Yang M, Shi W, Zhang H, Li W (2017) Evaluating soil dissolved organic matter extraction using three-dimensional excitation-emission matrix fluorescence spectroscopy. Pedosphere 27(5):968–973

    Google Scholar 

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Acknowledgements

This work was supported by NSF OIA 1556770. We thank the Vermont EPSCoR Basin Resilience to Extreme Events (BREE) collaborators for access to their field sites, facilities and equipment, and use of data. We also thank the University of Vermont Geology department and Rubenstein school faculty and staff for their expertise and assistance during this study.

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Correspondence to Julia N. Perdrial.

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Landsman-Gerjoi, M., Perdrial, J.N., Lancellotti, B. et al. Measuring the influence of environmental conditions on dissolved organic matter biodegradability and optical properties: a combined field and laboratory study. Biogeochemistry 149, 37–52 (2020). https://doi.org/10.1007/s10533-020-00664-9

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Keywords

  • Seasonal variability
  • Biodegradability
  • Dissolved organic matter
  • Fluorescence spectroscopy
  • PARAFAC