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Differential decomposition of humic acids by marine and estuarine bacterial communities at varying salinities

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Abstract

Humic substances (HS) constitute 50–80% of total dissolved organic matter (DOM) in freshwaters but in the open ocean <3%, indicating that large fractions of DOM and HS are removed in the estuarine and coastal zone. In order to assess the role of bacteria in this removal, we conducted experiments in flow-through cultures to examine the decomposition of peat bog-born humic acids (HA) by marine (salinity 30, Exp1) and estuarine (salinity 10, Exp2) bacterial communities. After ~70 days 40–>60% of the HA were decomposed. Highest fractions were decomposed in treatments in which the bacterial communities were fed by HA media of a foreign salinity, e.g., of 14 in Exp1 and of 28 in Exp2. Some of the HA material was not decomposed but broken down to smaller moieties entering the fulvic acid (FA) fraction. The analysis of the HA media and their residuals after bacterial decomposition by pyrolysis GC/MS showed that individual organic compounds were decomposed. In Exp1, 32 aliphatic and aromatic compounds, including lignin biomarkers, were detected in the HA medium of which mainly aliphatic compounds were decomposed. In Exp2, 49 compounds were detected of which ~40–60% were not detected any more after bacterial decomposition in the HA fraction but still in the FA fraction. The results show that estuarine and marine bacterial communities can decompose large amounts of HA and that this process is important in reducing the amount of terrestrial HS and DOM entering the estuarine and coastal region.

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References

  • Abril G, Nogueira M, Etcheber H, Cabeçadas, Lemaire E, Brogueiras MJ (2002) Behaviour of organic carbon in nine contrasting European estuaries. Est Coast Shelf Sci 54:241–262

    Article  Google Scholar 

  • Amon RMW, Benner R (1996) Bacterial utilization of different size classes of dissolved organic matter. Limnol Oceanogr 41:41–51

    Article  Google Scholar 

  • 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 Environ Microbiol 71:6267–6275

    Article  Google Scholar 

  • Bano N, Moran MA, Hodson RE (1997) Bacterial utilization of dissolved humic substances from a freshwater swamp. Aquat Microb Ecol 12:233–238

    Article  Google Scholar 

  • Bartholomä A, Kubicki A, Badewien T, Flemming BW (2009) Suspended sediment transport in the German Wadden Sea - seasonal variations and extreme events. Ocean Dyn 59:213–225

    Google Scholar 

  • Benner R (2002) Chemical composition and reactivity. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic Press, San Diego, pp 59–90

    Chapter  Google Scholar 

  • 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  Google Scholar 

  • Boyd TJ, Osborn CL (2004) Changes in CDOM fluorescence from allochthonous and autochthonous sources during tidal mixing and bacterial degradation in two coastal estuaries. Mar Chem 89:189–210

    Article  Google Scholar 

  • Bussmann I (1999) Bacterial utilization of humic substances from the Arctic Ocean. Aquat Microb Ecol 19:37–45

    Article  Google Scholar 

  • Cauwet G (2002) DOM in the coastal zone. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic Press, San Diego, pp 579–609

    Chapter  Google Scholar 

  • Chen ZQ, Hu CM, Comny RN, Muller-Karger F, Swarzenski P (2007) Colored dissolved organic matter in Tampa Bay, Florida. Mar Chem 104:98–109

    Article  Google Scholar 

  • Dittmar T, Kattner G (2003) Recalcitrant dissolved organic matter in the ocean: major contribution of small amphiphilics. Mar Chem 82:115–123

    Article  Google Scholar 

  • Donderski W, Burkowska A (2000) Metabolic activity of heterotrophic bacteria in the presence of humic substances and their fractions. Polish J Environ Studies 9:267–271

    Google Scholar 

  • Farjalla VF, Amado AM, Suhett AL, Meirelles-Pereira F (2009) DOC removal paradigms in highly humic aquatic ecosystems. Environ Sci Pollut Res 16:531–538

    Article  Google Scholar 

  • Fooken U, Liebezeit G (2000) Distinction of marine and terrestrial origin of humic acids in North Sea surface sediments by absorption spectroscopy. Mar Geol 164:173–181

    Article  Google Scholar 

  • Frazier SW, Kaplan LA, Hatcher PG (2005) Molecular characterization of biodegradable dissolved organic matter using bioreactors and [12C/13C] tetramethylammonium hydroxide thermochemolysis GC-MS. Environ Sci Technol 39:1479–1491

    Article  Google Scholar 

  • Gebhardt S (2005) Organic and geochemical investigations of streams of the Esens region in Eastern Frisia, Germany. PhD Thesis, Carl von Ossietzky Universität Oldenburg, Oldenburg (in German; http://www.oops.uni-oldenburg.de/volltexte/2005/149/)

  • Hatcher PG, Minnard RD (1996) Comparison of dehydrogenase polymer (DHP) lignin with native lignin from gymnosperm wood by thermochemolysis using tetramethylammonium hydroxide (TMAH). Org Geochem 24:593–600

    Article  Google Scholar 

  • Hedges JI, Keil RG, Benner R (1997) What happens to terrestrial organic matter in the ocean? Org Geochem 27:195–212

    Article  Google Scholar 

  • Hubberten U, Lara RJ, Kattner G (1994) Amino acid composition of seawater and dissolved humic substances in the Greenland Sea. Mar Chem 45:121–128

    Article  Google Scholar 

  • Kaiser K, Guggenberger G (2000) The role of DOM sorption to mineral surfaces in the preservation of organic matter in soils. Organic Geochem 31:711–725

    Google Scholar 

  • Kisand V, Rocker D, Simon M (2008) Significant decomposition of riverine humic-rich DOC by marine but not estuarine bacteria assessed in sequential chemostat experiments. Aquat Microb Ecol 53:151–160

    Article  Google Scholar 

  • Koch BP, Witt M, Engbrodt R, Dittmar T, Kattner G (2005) Molecular formulae of marine and terrigenous dissolved organic matter detected by electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. Geochim Cosmochim Acta 69:3299–3308

    Article  Google Scholar 

  • Kulovaara M (1996) Light-induced degradation of aquatic humic substances by simulated sunlight. Internat J Environ Anal Chem 62:85–95

    Article  Google Scholar 

  • Lehtonen T, Peuravouri J, Pihlaja K (2000) Characterisation of lake-aquatic humic matter isolated with two different sorbing solid techniques: tetramethylammonium hydroxide treatment and pyrolysis-gas chromatography/mass spectrometry. Anal Chim Acta 424:91–103

    Article  Google Scholar 

  • Loh AN, Bauer JE, Druffel ERM (2004) Variable ageing and storage of dissolved organic components in the open ocean. Nature 430:877–881

    Article  Google Scholar 

  • Lübben A, Dellwig O, Koch S, Beck M, Badewien TH, Fischer S, Reuter R (2009) Distributions and characteristics of dissolved organic matter in temperate coastal waters (Southern North Sea). Ocean Dyn 59:263–275

    Article  Google Scholar 

  • Lunau M, Lemke A, Dellwig O, Simon M (2006) Physical and biogeochemical controls of microaggregate dynamics in a tidally affected coastal ecosystem. Limnol Oceanogr 51:847–859

    Google Scholar 

  • Malcolm RL, MacCarthy P (1992) Quantitative evaluation of XAD-8 and XAD-4 resins used in tandem for removing organic solutes from water. Environ Int 18:597–607

    Article  Google Scholar 

  • Martin F, del Rio JC, González-Vila FJ, Verdejo T (1995) Pyrolysis derivatization of humic substances 2. Pyrolysis of soil humic acids in the presence of tetramethylammonium hydroxide. J Anal Appl Pyrolysis 31:75–83

    Article  Google Scholar 

  • McKnight DM, Aiken GR (1998) Sources and age of aquatic humus. In: Hessen DO, Tranvik LJ (eds) Aquatic humic substances. Ecology and biochemistry. Springer, New York, pp 9–39

    Chapter  Google Scholar 

  • Miller WL, Moran MA (1997) Interaction of photochemical and microbial processes in the degradation of refractory dissolved organic matter from a coastal marine environment. Limnol Oceanogr 42:1317–1324

    Article  Google Scholar 

  • Mopper K, Kieber DJ (2002) Photochemistry and the cycling of carbon, sulfur, nitrogen, and phosphorus. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic Press, San Diego, pp 455–507

    Chapter  Google Scholar 

  • Moran MA, Sheldon WM, Zepp RG (2000) Carbon loss and optical property changes during long-term photochemical and biological degradation of estuarine dissolved organic matter. Limnol Oceanogr 45:1254–1264

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Obernosterer I, Herndl GJ (2000) Differences in the optical and biological reactivity of the humic and nonhumic dissolved organic carbon component in two contrasting coastal marine environments. Limnol Oceanogr 45:1120–1129

    Article  Google Scholar 

  • Opsahl S, Benner R (1997) Distribution and cycling of terrigenous dissolved organic matter in the ocean. Nature 386:480–482

    Article  Google Scholar 

  • Page DW, van Leeuwen JA, Spark KM, Mulcahy DE (2001) Tracing terrestrial compounds leaching from two reservoir catchments as input to dissolved organic matter. Mar Freshwater Res 52:223–233

    Article  Google Scholar 

  • Poerschmann J, Kopinke F-D, Balcke G, Mothes S (1997) Pyrolysis pattern of anthropogenic and natural humic organic matter. J Micricolumn Separations 10:401–411

    Article  Google Scholar 

  • Poerschmann J, Trommler U, Fabbri D, Gorecki T (2007) Combined application of non-discriminated conventional pyrolysis and tetramethylammonium hydroxide-induced thermochemolysis for the characterization of the molecular structure of humic acid isolated from polluted sediments from the Ravenna Lagoon. Chemosphere 70:196–205

    Article  Google Scholar 

  • 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  Google Scholar 

  • Rocker D, Brinkhoff T, Grüner N, Dogs M, Simon M (2011) Composition of humic acid degrading estuarine and marine bacterial communities. FEMS Microbiol Ecol, resubmitted

  • Rosenstock B, Simon M (2003) Consumption of dissolved amino acids and carbohydrates by limnetic bacterioplankton according to molecular weight fractions and proportions bound to humic matter. Microb Ecol 45:433–443

    Article  Google Scholar 

  • Rosenstock B, Zwisler W, Simon M (2005) Bacterial consumption of humic and non-humic low and high molecular weight DOM and the effect of solar irradiation on the turnover of amino acids and carbohydrates in the Southern Ocean. Microb Ecol 50:90–101

    Article  Google Scholar 

  • Schulten HR, Gleixner G (1999) Analytical pyrolysis of humic substances and dissolved organic matter in aquatic systems: structure and origin. Water Res 33:2489–2498

    Article  Google Scholar 

  • Schulten HR, Sorge C (1995) Pyrolysis methylation—mass spectrometry of whole soils. Eur J Soil Sci 46:567–579

    Article  Google Scholar 

  • Sholkovitz ER (1976) Flocculation of dissolved organic and inorganic matter during the mixing of river water and seawater. Geochim Cosmochim Acta 40:831–845

    Article  Google Scholar 

  • Sholkovitz ER, Boyle EA, Price NB (1978) The removal of dissolved humic acids and iron during estuarine mixing. Earth Planet Sci Letters 41:77–86

    Article  Google Scholar 

  • Simon M, Azam F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51:201–213

    Article  Google Scholar 

  • Stevens H, Brinkhoff T, Rink B, Vollmers J, Simon M (2007) Diversity and abundance of gram-positive bacteria in a tidal flat ecosystem. Environ Microb 9:1810–1822

    Article  Google Scholar 

  • Thurman EM (1985) Organic geochemistry of natural waters. Nijhoff/Junk Publishers, Boston

    Book  Google Scholar 

  • Thurman EM, Malcolm RL (1981) Preparative isolation of aquatic humic substances. Environ Sci Technol 15:463–466

    Article  Google Scholar 

  • Uher G, Hughes C, Henry G, Upstill-Goddard RC (2001) Non-conservative mixing behavior of colored dissolved organic matter in a humic-rich, turbid estuary. Geophys Res Let 28:3309–3312

    Article  Google Scholar 

  • Van de Meent D, Brown SC, Philp RP, Simoneit BRT (1980) Pyrolysis-high resolution gas chromatography and pyrolysis gas chromatography-mass spectrometry of kerogens and kerogen precursors. Geochim Cosmochim Acta 44:999–1013

    Article  Google Scholar 

  • Warnock RE, Gieskes WWC, van Laar S (1999) Regional and seasonal differences in light absorption by yellow substance in the Southern Bight of the North Sea. J Sea Res 42:169–178

    Article  Google Scholar 

  • Wikner J, Cuadros R, Jansson M (1999) Differences in consumption of allochthonous DOC between a lake and an estuary in a temperate watershed. Aquat Microb Ecol 17:289–299

    Article  Google Scholar 

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Acknowledgments

We are most grateful to A. Schlingloff for DOC analyses. We thank B. Kuerzel for help with the flow cytometric analyses of bacterial numbers and to H. Simon for assistance in sample collection. This work was supported by grant Si 360/22-1 from Deutsche Forschungsgemeinschaft (DFG). V. Kisand was supported by the European Regional Development Fund through the Center of Excellence in Chemical Biology, Estonia.

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Correspondence to Meinhard Simon.

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Rocker, D., Kisand, V., Scholz-Böttcher, B. et al. Differential decomposition of humic acids by marine and estuarine bacterial communities at varying salinities. Biogeochemistry 111, 331–346 (2012). https://doi.org/10.1007/s10533-011-9653-4

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