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Disentangling the Interactions Between Photochemical and Bacterial Degradation of Dissolved Organic Matter: Amino Acids Play a Central Role

Abstract

Photochemical and bacterial degradation are important pathways to carbon mineralization and can be coupled in dissolved organic matter (DOM) decomposition. However, details of several mechanisms of the coupled photochemical and biological processing of DOM remain too poorly understood to achieve accurate predictions of the impact of these processes on DOM fate and reactivity. The aim of this study was to evaluate how photochemical degradation of amino acids affects bacterial metabolism and whether or not photochemical degradation of DOM competes for amino acids with biological processes. We examined the interactions between photochemical and bacterial degradation dynamics using a mixture of 18 amino acids and examined their dynamics and turnover rates within a larger pool of allochthonous or autochthonous DOM. We observed that photochemical exposure of DOM containing amino acids led to delayed biomass production (even though the final biomass did not differ), most likely due to a need for upregulation of biosynthetic pathways for amino acids that were damaged by photochemically produced reactive oxygen species (ROS). This response was most pronounced in bacterial communities where the abundance of photosensitive amino acids was highest (amended treatments and autochthonous DOM) and least pronounced when the abundance of these amino acids was low (unamended and allochthonous DOM), likely because these bacteria already had these biosynthetic pathways functioning. We observed both a cost and benefit associated with photochemical exposure of DOM. We observed a cost associated with photochemically produced ROS that partially degrade key amino acids and a benefit associated with an increase in the availability of other compounds in the DOM. Bacteria growing on DOM sources that are low in labile amino acids, such as those in terrestrially influenced environments, experience more of the benefits associated with photochemical exposure, whereas bacteria growing in more amino acid-rich environments, such as eutrophic and less terrestrially influenced waters, experience a higher cost due to the increased necessity of salvage pathways for these essential amino acids. Finally, we propose a conceptual model whereby the effects of DOM photochemical degradation on microbial metabolism result from the balance between two mechanisms: One is dependent on the DOM sources, and the other is dependent on the DOM concentration in natural systems.

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References

  1. 1.

    Farrington J (1992) Overview and key recommendations—marine organic geochemistry workshop, January 1990. Mar Chem 39:5–9

    Article  Google Scholar 

  2. 2.

    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 10:171–184

    Article  CAS  Google Scholar 

  3. 3.

    Tranvik L, Downing JA, Cotner JB, Loiselle SA, Striegl RG, Ballatore TJ, Dillon P, Finlay K, Fortino K, Knoll LB, Kortelainen PL, Kutser T, Larsen S, Laurion I, Leech DM, McCallister SL, McKnight DM, Melack JM, Overholt E, Porter JA, Prairie Y, Renwick WH, Roland F, Sherman BS, Schindler DW, Sobek S, Tremblay A, Vanni MJ, Verschoor AM, Wachenfeldt A, Weyhenmeyer GA (2009) Lakes and reservoirs as regulators of carbon cycling and climate. Limnol Oceanogr 54:2298–2314

    Article  CAS  Google Scholar 

  4. 4.

    Raymond PA, Hartmann J, Lauerwald R, Sobek S, McDonald C, Hoover M, Butman D, Striegl R, Mayorga E, Humborg C, Kortelainen P, Dürr H, Meybeck M, Ciais P, Guth P (2013) Global carbon dioxide emissions from inland waters. Nature 503:355–359

    Article  CAS  PubMed  Google Scholar 

  5. 5.

    Ruiz-Gonzáles C, Simó R, Sommaruga R, Gasol JM (2013) Away from darkness: a review on the effects of solar radiation on heterotrophic bacterioplankton activity. Front Microbiol 4:131

    Google Scholar 

  6. 6.

    Amado AM, Farjalla VF, Esteves FD, Bozelli RL, Roland F, Enrich-Prast A (2006) Complementary pathways of dissolved organic carbon removal pathways in clear-water Amazonian ecosystems: photochemical degradation and bacterial uptake. FEMS Microbiol Ecol 56:8–17

    Article  CAS  PubMed  Google Scholar 

  7. 7.

    Cory RM, Ward CP, Crump BC, Kling GW (2014) Sunlight controls water column processing of carbon in arctic fresh waters. Science 345:925–928

    Article  CAS  PubMed  Google Scholar 

  8. 8.

    Jonsson A, Meili M, Bergstrom AK, Jansson M (2001) Whole-lake mineralization of allochthonous and autochthonous organic carbon in a large humic lake (Ortrasket, N. Sweden). Limnol Oceanogr 46:1691–1700

    Article  CAS  Google Scholar 

  9. 9.

    Vahatalo AV, Wetzel RG (2008) Long-term photochemical and microbial decomposition of wetland-derived dissolved organic matter with alteration of C-13: C-12 mass ratio. Limnol Oceanogr 53:1387–1392

    Article  CAS  Google Scholar 

  10. 10.

    Amado AM, Cotner JB, Suhett AL, Esteves FA, Bozelli RL, Farjalla VF (2007) Contrasting interactions mediate dissolved organic matter decomposition in tropical aquatic ecosystems. Aquat Microb Ecol 49:25–34

    Article  Google Scholar 

  11. 11.

    Obernosterer I, Benner R (2004) Competition between biological and photochemical processes in the mineralization of dissolved organic carbon. Limnol Oceanogr 49:117–124

    Article  CAS  Google Scholar 

  12. 12.

    Cory RM, Kaplan LA (2012) Biological lability of streamwater fluorescent dissolved organic matter. Limnol Oceanogr 57:1347–1380

    Article  CAS  Google Scholar 

  13. 13.

    Nieto-Cid M, Alvarez-Salgado XA, Perez FF (2006) Microbial and photochemical reactivity of fluorescent dissolved organic matter in a coastal upwelling system. Limnol Oceanogr 51:1391–1400

    Article  CAS  Google Scholar 

  14. 14.

    Benner R, Biddanda B (1998) Photochemical transformations of surface and deep marine dissolved organic matter: effects on bacterial growth. Limnol Oceanogr 43:1373–1378

    Article  CAS  Google Scholar 

  15. 15.

    Kragh T, Sondergaard M, Tranvik L (2008) Effect of exposure to sunlight and phosphorus-limitation on bacterial degradation of coloured dissolved organic matter (CDOM) in freshwater. FEMS Microbiol Ecol 64:230–239

    Article  CAS  PubMed  Google Scholar 

  16. 16.

    Cotner JB, Biddanda BA (2002) Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5:105–121

    Article  CAS  Google Scholar 

  17. 17.

    Anesio AM, Graneli W, Aiken GR, Kieber DJ, Mopper K (2005) Effect of humic substance photodegradation on bacterial growth and respiration in lake water. Appl Environm Microbiol 71:6267–6275

    Article  CAS  Google Scholar 

  18. 18.

    Pullin MJ, Bertilsson S, Goldstone JV, Voelker BM (2004) Effects of sunlight and hydroxyl radical on dissolved organic matter: bacterial growth efficiency and production of carboxylic acids and other substrates. Limnol Oceanogr 49:2011–2022

    Article  CAS  Google Scholar 

  19. 19.

    Tranvik LJ, Bertilsson S (2001) Contrasting effects of solar UV radiation on dissolved organic sources for bacterial growth. Ecol Lett 4:458–463

    Article  Google Scholar 

  20. 20.

    Boreen AL, Edhlund BL, Cotner JB, McNeill K (2008) Indirect photodegradation of dissolved free amino acids: the contribution of singlet oxygen and the differential reactivity of DOM from various sources. Environm Sci Technol 42:5492–5498

    Article  CAS  Google Scholar 

  21. 21.

    Latch DE, McNeill K (2006) Microheterogeneity of singlet oxygen distributions in irradiated humic acid solutions. Science 311:1743–1747

    Article  CAS  PubMed  Google Scholar 

  22. 22.

    Cory RM, McNeill K, Cotner JP, Amado A, Purcell JM, Marshall AG (2010) Singlet oxygen in the coupled photochemical and biochemical oxidation of dissolved organic matter. Environm Sci Technol 44:3683–3689

    Article  CAS  Google Scholar 

  23. 23.

    Averett RC, Leenheer JA, McKnight DM, Thorn KA (1994) Humic substances in the Suwannee River, Georgia: interactions, properties, and proposed structures. USGS, Denver

    Google Scholar 

  24. 24.

    Stenson AC, Marshall AG, Cooper WT (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 75:1275–1284

    Article  CAS  PubMed  Google Scholar 

  25. 25.

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

    Article  CAS  Google Scholar 

  26. 26.

    Cawley K, McKnight DM, Miller PL, Cory RM, Fimmen R, Geurard J, Dieser M, Jaros C, Chin YP, Foreman CF (2013) Characterization of fulvic acid fractions of dissolved organic matter during ice-out in a hyper-eutrophic, coastal pond in Antarctica. Environ Res Lett 8:1–10

    Article  Google Scholar 

  27. 27.

    Wetzel RG, Likens GE (1990) Limnological analyzes. Springer, New York

    Google Scholar 

  28. 28.

    Briand E, Pringault O, Jacquet S, Torreton JP (2004) The use of oxygen microprobes to measure bacterial respiration for determining bacterioplankton growth efficiency. Limnol Oceanogr Methods 2:406–416

    Article  Google Scholar 

  29. 29.

    Biddanda B, Ogdahl M, Cotner J (2001) Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol Oceanogr 46:730–739

    Article  Google Scholar 

  30. 30.

    Berggren M, Lapierre JF, del Giorgio PA (2012) Magnitude and regulation of bacterioplankton respiratory quotient across freshwater environmental gradients. Isme J 6:984–993

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. 31.

    del Giorgio PA, Bird DF, Prairie YT, Planas D (1996) Flow cytometric determination of bacterial abundance in lake plankton with the green nucleic acid stain SYTO 13. Limnol Oceanogr 41:783–789

    Article  Google Scholar 

  32. 32.

    Theil-Nielsen J, Sondergaard M (1998) Bacterial carbon biomass calculated from biovolumes. Arch Hydrobiol 141:195–207

    CAS  Google Scholar 

  33. 33.

    Lakowicz JR (1999) Principles of Fluorescence Spectroscopy. Kluwer, New York

    Book  Google Scholar 

  34. 34.

    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 46:38–48

    Article  CAS  Google Scholar 

  35. 35.

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

    Article  CAS  Google Scholar 

  36. 36.

    Stedmon CA, Bro R (2008) Characterizing dissolved organic matter fluorescence with parallel factor analysis: a tutorial. Limnology and Oceanography-Methods 6:572–579

    Article  CAS  Google Scholar 

  37. 37.

    Cory RM, Cotner JB, McNeill K (2009) Quantifying interactions between singlet oxygen and aquatic fulvic acids. Environm Sci Technol 43:718–723

    Article  CAS  Google Scholar 

  38. 38.

    Paul A, Hackbarth S, Vogt RD, Roder B, Burnison BK, Steinberg CEW (2004) Photogeneration of singlet oxygen by humic substances: comparison of humic substances of aquatic and terrestrial origin. Photochem Photobiol Sci 3:273–280

    Article  CAS  PubMed  Google Scholar 

  39. 39.

    Sulzberger B, Durisch-Kaiser E (2009) Chemical characterization of dissolved organic matter (DOM): a prerequisite for understanding UV-induced changes of DOM absorption properties and bioavailability. Aquat Sci 71:104–126

    Article  CAS  Google Scholar 

  40. 40.

    Benner R, Kaiser K (2011) Biological and photochemical transformations of amino acids and lignin phenols in riverine dissolved organic matter. Biogeochemistry 102:209–222

    Article  CAS  Google Scholar 

  41. 41.

    Thorn KA, Cox LG (2009) N-15 NMR spectra of naturally abundant nitrogen in soil and aquatic natural organic matter samples of the international humic substances society. Org Geochem 40:484–499

    Article  CAS  Google Scholar 

  42. 42.

    Kieber RJ, Zhou XL, Mopper K (1990) Formation of carbonyl-compounds from Uv-induced photodegradation of humic substances in natural-waters—fate of riverine carbon in the sea. Limnol Oceanogr 35:1503–1515

    Article  CAS  Google Scholar 

  43. 43.

    Zepp RG, Wolfe NL, Baughman GL, Hollis RC (1977) Singlet oxygen in natural-waters. Nature 267:421–423

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation under grant number OCE-0527196. A.M.A. is thankful to CNPq for the Scholarship from Sandwich Program (SWE Proc. # 200961/2005-5). Thanks to Meghan Jacobson, Andrea Little, and Mark Lunzer for Laboratory assistance and to A. Dean for kindly allowing use of their flow cytometer for bacterial cell counts.

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Correspondence to André M. Amado.

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Amado, A.M., Cotner, J.B., Cory, R.M. et al. Disentangling the Interactions Between Photochemical and Bacterial Degradation of Dissolved Organic Matter: Amino Acids Play a Central Role. Microb Ecol 69, 554–566 (2015). https://doi.org/10.1007/s00248-014-0512-4

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Keywords

  • Photochemical degradation
  • Bacterial degradation
  • Dissolved organic matter
  • Amino acids