Microbial Ecology

, Volume 64, Issue 3, pp 593–604 | Cite as

Labile and Recalcitrant Organic Matter Utilization by River Biofilm Under Increasing Water Temperature

  • Irene YllaEmail author
  • Anna M. Romaní
  • Sergi Sabater
Microbiology of Aquatic Systems


Microbial biofilms in rivers contribute to the decomposition of the available organic matter which typically shows changes in composition and bioavailability due to their origin, seasonality, and watershed characteristics. In the context of global warming, enhanced biofilm organic matter decomposition would be expected but this effect could be specific when either a labile or a recalcitrant organic matter source would be available. A laboratory experiment was performed to mimic the effect of the predicted increase in river water temperature (+4 °C above an ambient temperature) on the microbial biofilm under differential organic matter sources. The biofilm microbial community responded to higher water temperature by increasing bacterial cell number, respiratory activity (electron transport system) and microbial extracellular enzymes (extracellular enzyme activity). At higher temperature, the phenol oxidase enzyme explained a large fraction of respiratory activity variation suggesting an enhanced microbial use of degradation products from humic substances. The decomposition of hemicellulose (β-xylosidase activity) seemed to be also favored by warmer conditions. However, at ambient temperature, the enzymes highly responsible for respiration activity variation were β-glucosidase and leu-aminopeptidase, suggesting an enhanced microbial use of polysaccharides and peptides degradation products. The addition of labile dissolved organic carbon (DOC; dipeptide plus cellobiose) caused a further augmentation of heterotrophic biomass and respiratory activity. The changes in the fluorescence index and the ratio Abs250/total DOC indicated that higher temperature accelerated the rates of DOC degradation. The experiment showed that the more bioavailable organic matter was rapidly cycled irrespective of higher temperature while degradation of recalcitrant substances was enhanced by warming. Thus, pulses of carbon at higher water temperature might have consequences for DOC processing.


Dissolve Organic Carbon Concentration Dissolve Organic Matter Phenol Oxidase Extracellular Enzyme Activity Community Respiration 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This study was funded by projects CGL2007-65549/BOS, CGL2008-05618-C02/BOS, CGL2011-30151-C02-01, and SCARCE (Consolider-Ingenio CSD2009-00065) of the Spanish Ministry of Economy and Competitiveness. We thank Juanita Mora for her help in the laboratory analysis and Helmut Fischer for his advice on DOC quality interpretation. We also thank four anonymous reviewers for their suggestions.


  1. 1.
    Acuña V, Tockner K (2010) The effects of alterations in temperature and flow regime on organic carbon dynamics in Mediterranean river networks. Glob Chang Biol 16:2638–2650Google Scholar
  2. 2.
    Amon RMW, Benner R (1996) Bacterial utilization of different size classes of dissolved organic matter. Limnol Oceanogr 41(1):41–51CrossRefGoogle Scholar
  3. 3.
    Andrews JA, Matamala R, Westover KM, Schlesinger WH (2000) Temperature effects on the diversity of soil heterotrophs and the delta C-13 of soil-respired CO2. Soil Biol Biochem 32(5):699–706CrossRefGoogle Scholar
  4. 4.
    Artigas J, Romaní AM, Gaudes A, Muñoz I, Sabater S (2009) Organic matter availability structures microbial biomass and activity in a Mediterranean stream. Freshw Biol 54(10):2025–2036CrossRefGoogle Scholar
  5. 5.
    Artigas J, Romani AM, Sabater S (2008) Relating nutrient molar ratios of microbial attached communities to organic matter utilization in a forested stream. Fundam Appl Limnol 173(3):255–264CrossRefGoogle Scholar
  6. 6.
    Baulch HM, Schindler DW, Turner MA, Findlay DL, Paterson MJ, Vinebrooke RD (2005) Effects of warming on benthic communities in a boreal lake: implications of climate change. Limnol Oceanogr 50(5):1377–1392CrossRefGoogle Scholar
  7. 7.
    Berggren M, Laudon H, Jonsson A, Jansson M (2010) Nutrient constraints on metabolism affect the temperature regulation of aquatic bacterial growth efficiency. Microb Ecol 60:894–902PubMedCrossRefGoogle Scholar
  8. 8.
    Bertilsson S, Tranvik LJ (2000) Photochemical transformation of dissolved organic matter in lakes. Limnol Oceanogr 45(4):753–762CrossRefGoogle Scholar
  9. 9.
    Bianchi TS, Filley T, Dria K, Hatcher PG (2004) Temporal variability in sources of dissolved organic carbon in the lower Mississippi River. Geochim Cosmochim Acta 68(5):959–967CrossRefGoogle Scholar
  10. 10.
    Blenkinsopp SA, Lock MA (1990) The measurement of electron-transport system activity in river biofilms. Water Res 24(4):441–445CrossRefGoogle Scholar
  11. 11.
    Cabaniss SE, Madey G, Leff L, Maurice PA, Wetzel R (2005) A stochastic model for the synthesis and degradation of natural organic matter. Part I. Data structures and reaction kinetics. Biogeochemistry 76(2):319–347CrossRefGoogle Scholar
  12. 12.
    Claret C (1998) Hyporrheic biofilm development on artificial substrate, as a tool for assessing trophic status of aquatic systems: first results. Ann Limnol -Int J Lim 34(2):119–128CrossRefGoogle Scholar
  13. 13.
    Conant RT, Drijber RA, Haddix ML, Parton WJ, Paul EA, Plante AF, Six J, Steinweg JM (2008) Sensitivity of organic matter decomposition to warming varies with its quality. Glob Chang Biol 14(4):868–877CrossRefGoogle Scholar
  14. 14.
    Conen F, Leifeld J, Seth B, Alewell C (2006) Warming mineralises young and old soil carbon equally. Biogeosciences 3(4):515–519CrossRefGoogle Scholar
  15. 15.
    Chróst RJ, Overbeck J (1990) Substrate ectoenzyme interaction: significance of beta-glucosidase activity for glucose-metabolism by aquatic bacteria. Arch Hydrobiol 34:93–98Google Scholar
  16. 16.
    Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440(7081):165–173PubMedCrossRefGoogle Scholar
  17. 17.
    De Haan H (1993) Solar UV-light penetration and photodegradation of humic substances in peaty lake water. Limnol Oceanogr 38(5):1072–1076CrossRefGoogle Scholar
  18. 18.
    Deshpande V, Eriksson KE (1988) 1,4-beta-glucosidases of Sporotrichum pulverulentum. Methods Enzymol 160:415–424CrossRefGoogle Scholar
  19. 19.
    Díaz V, Font J, Schwartz T, Romaní AM (2011) Biofilm formation at warming temperature: acceleration of microbial colonization and microbial interactive effects. Biofouling 27(1):59–71CrossRefGoogle Scholar
  20. 20.
    Fang CM, Smith P, Moncrieff JB, Smith JU (2005) Similar response of labile and resistant soil organic matter pools to changes in temperature. Nature 433(7021):57–59PubMedCrossRefGoogle Scholar
  21. 21.
    Fenner N, Freeman C, Lock MA, Harmens H, Reynolds B, Sparks T (2007) Interactions between elevated CO2 and warming could amplify DOC exports from peatland catchments. Environ Sci Technol 41:3146–3152PubMedCrossRefGoogle Scholar
  22. 22.
    Findlay S, Sinsabaugh RL, Sobczak WV, Hoostal M (2003) Metabolic and structural response of hyporheic microbial communities to variations in supply of dissolved organic matter. Limnol Oceanogr 48(4):1608–1617CrossRefGoogle Scholar
  23. 23.
    Fischer H (2003) The role of biofilms in the uptake and transformation of dissolved organic matter. In: Findlay SEG, Sinsabaugh RL (eds) Aquatic ecosystems: interactivity of dissolved organic matter. Academic, San Diego, pp 285–313Google Scholar
  24. 24.
    Fischer H, Mille-Lindblom C, Zwirnmann E, Tranvik LJ (2006) Contribution of fungi and bacteria to the formation of dissolved organic carbon from decaying common reed (Phragmites australis). Arch Hydrobiol 166(1):79–97CrossRefGoogle Scholar
  25. 25.
    Francoeur SN, Wetzel RG (2003) Regulation of periphytic leucine-aminopeptidase activity. Aquat Microb Ecol 31(3):249–258CrossRefGoogle Scholar
  26. 26.
    Freeman C, Lock MA, Marxsen J, Jones SE (1990) Inhibitory effects of high molecular weight dissolved organic matter on metabolic processes in contrasted rivers and streams. Freshw Biol 24:159–166CrossRefGoogle Scholar
  27. 27.
    Freese HM, Karsten U, Schumannn R (2006) Bacterial abundance, activity, and viability in the eutrophic river Warnow, Northeast Germany. Microb Ecol 51:117–127PubMedCrossRefGoogle Scholar
  28. 28.
    Giardina CP, Ryan MG (2000) Evidence that decomposition rates of organic carbon in mineral soil do not vary with temperature. Nature 404(6780):858–861PubMedCrossRefGoogle Scholar
  29. 29.
    Guasch H, Sabater S (1995) Seasonal variations in photosynthesis—irradiance responses by biofilms in Mediterranean streams. J Phycol 31(5):727–735CrossRefGoogle Scholar
  30. 30.
    Gudasz C, Bastviken D, Steger K, Premke K, Sobek S, Tranvik LJ (2010) Temperature-controlled organic carbon mineralization in lake sediments. Nature 466:479–481Google Scholar
  31. 31.
    Guenet B, Danger M, Abbadie L, Lacroix G (2010) Priming effect: bridging the gap between terrestrial and aquatic ecology. Ecology 91(10):2850–2861PubMedCrossRefGoogle Scholar
  32. 32.
    Hach (1992) Water analysis handbook, 2nd edn. Hach, Loveland, COGoogle Scholar
  33. 33.
    IPCC (2007) Summary for policymakers. Cambridge University Press, CambridgeGoogle Scholar
  34. 34.
    Jackson TA, Hecky RE (1980) Depression of primary productivity by humic matter in lake and reservoir waters of the boreal forest zone. Can J Fish Aquat Sci 37(12):2300–2317CrossRefGoogle Scholar
  35. 35.
    Jansson M, Blomqvist P, Jonsson A, Bergstrom AK (1996) Nutrient limitation of bacterioplankton, autotrophic and mixotrophic phytoplankton, and heterotrophic nanoflagellates in Lake Ortrasket. Limnol Oceanogr 41(7):1552–1559CrossRefGoogle Scholar
  36. 36.
    Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher-plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167(2):191–194Google Scholar
  37. 37.
    Jenkinson DS, Adams DE, Wild A (1991) Model estimates of CO2 emissions from soil in response to global warming. Nature 351(6324):304–306CrossRefGoogle Scholar
  38. 38.
    Kaplan LA, Newbold JD (2003) The role of monomers in stream ecosystem metabolism. In: Findlay SEG, Sinsabaugh RL (eds) Aquatic ecosystems: interactivity of dissolved organic matter. Academic, San Diego, pp 99–119Google Scholar
  39. 39.
    Kathol M, Norf H, Arndt H, Weitere M (2009) Effects of temperature increase on the grazing of planktonic bacteria by biofilm-dwelling consumers. Aquat Microb Ecol 55(1):65–79CrossRefGoogle Scholar
  40. 40.
    Knorr W, Prentice IC, House JI, Holland EA (2005) Long-term sensitivity of soil carbon turnover to warming. Nature 433(7023):298–301PubMedCrossRefGoogle Scholar
  41. 41.
    Krasner SW, Westerhoff P, Chen B, Rittmann BE, Nam S-N, Amy G (2009) Impact of wastewater treatment processes on organic carbon, organic nitrogen, and DBP precursors in effluent organic matter. Environ Sci Technol 43(8):2911–2918PubMedCrossRefGoogle Scholar
  42. 42.
    Kritzberg ES, Cole JJ, Pace ML, Granéli W, Bade DL (2004) Autochthonous versus allochthonous carbon sources of bacteria: results from whole-lake 13C addition experiments. Limnol Oceanogr 49(2):588–596CrossRefGoogle Scholar
  43. 43.
    Lachke AH (1988) 1,4-beta-d-xylan xylohydrolase of Sclerotium rolfsii. Methods Enzymol 160:679–684CrossRefGoogle Scholar
  44. 44.
    McCallister SL, del Giorgio PA (2998) Direct measurement of the δ13C signature of carbon respired by bacteria in lakes: linkages to potential carbon sources, ecosystem baseline metabolism, and CO2 fluxes. Limnol Oceanogr 53(4):1204–1216CrossRefGoogle Scholar
  45. 45.
    McDonald S, Bishop AG, Prenzler PD, Robards K (2004) Analytical chemistry of freshwater humic substances. Anal Chim Acta 527(2):105–124CrossRefGoogle Scholar
  46. 46.
    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):38–48CrossRefGoogle Scholar
  47. 47.
    Meyer JL (1994) The microbial loop in flowing waters. Microb Ecol 28(2):195–199CrossRefGoogle Scholar
  48. 48.
    Meyer JL, Edwards RT, Risley R (1987) Bacterial growth on dissolved organic carbon from a blackwater river. Microb Ecol 13:13–29CrossRefGoogle Scholar
  49. 49.
    Morris DP, Hargreaves BR (1997) The role of photochemical degradation of dissolved organic carbon in regulating the UV transparency of three lakes on the Pocono Plateau. Limnol Oceanogr 42(2):239–249CrossRefGoogle Scholar
  50. 50.
    Murphy J, Riley JP (1962) A modified single solution for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36CrossRefGoogle Scholar
  51. 51.
    Peter H, Ylla I, Gudasz C, Romaní AM, Sabater S, Tranvik L (2011) Multifunctionality and diversity in bacterial biofilms. PLoS One 6(8):e23225PubMedCrossRefGoogle Scholar
  52. 52.
    Piccolo A (2001) The supramolecular structure of humic substances. Soil Sci 166(11):810–832CrossRefGoogle Scholar
  53. 53.
    Porcal P, Koprivnjak JF, Molot LA, Dillon PJ (2009) Humic substances-part 7: the biogeochemistry of dissolved organic carbon and its interactions with climate change. Environ Sci Pollut Res 16(6):714–726CrossRefGoogle Scholar
  54. 54.
    Reichstein M, Katterer T, Andren O, Ciais P, Schulze ED, Cramer W, Papale D, Valentini R (2005) Temperature sensitivity of decomposition in relation to soil organic matter pools: critique and outlook. Biogeosciences 2(4):317–321CrossRefGoogle Scholar
  55. 55.
    Romaní AM, Artigas J, Ylla I (2012) Extracellular enzymes in aquatic biofilms: microbial interactions versus water quality effects in the use of organic matter. In: Lear G, Lewis GD (eds) Microbial biofilms: current research and applications. Caister Academic Press, New ZealandGoogle Scholar
  56. 56.
    Romaní AM, Guasch H, Muñoz I, Ruana J, Vilalta E, Schwartz T, Emtiazi F, Sabater S (2004) Biofilm structure and function and possible implications for riverine DOC dynamics. Microb Ecol 47(4):316–328PubMedCrossRefGoogle Scholar
  57. 57.
    Romaní AM, Vázquez E, Butturini A (2006) Microbial availability and size fractionation of dissolved organic carbon after drought in an intermittent stream: biogeochemical link across the stream-riparian interface. Microb Ecol 52(3):501–512PubMedCrossRefGoogle Scholar
  58. 58.
    Sand-Jensen K, Pedersen NL, Sondergaard M (2007) Bacterial metabolism in small temperate streams under contemporary and future climates. Freshw Biol 52:2340–2353CrossRefGoogle Scholar
  59. 59.
    Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404CrossRefGoogle Scholar
  60. 60.
    Sinsabaugh RL, Osgood MP, Findlay S (1994) Enzymatic models for estimating decomposition rates of particulate detritus. J N Am Bentholl Soc 13(2):160–169CrossRefGoogle Scholar
  61. 61.
    Thornley JHM, Cannell MGR (2001) Soil carbon storage response to temperature: an hypothesis. Ann Bot 87(5):591–598CrossRefGoogle Scholar
  62. 62.
    Tranvik LJ (1988) Availability of dissolved organic carbon for planktonic bacteria in oligotrophic lakes of differing humic content. Microb Ecol 16(3):311–322CrossRefGoogle Scholar
  63. 63.
    Vázquez E, Amalfitano S, Fazi S, Butturini A (2011) Dissolved organic matter composition in a fragmented Mediterranean fluvial system under severe drought conditions. Biogeochemistry 102:50–72CrossRefGoogle Scholar
  64. 64.
    Vázquez E, Romaní AM, Sabater F, Butturini A (2007) Effects of the dry-wet hydrological shift on dissolved organic carbon dynamics and fate across stream-riparian interface in a Mediterranean catchment. Ecosystems 10(2):239–251CrossRefGoogle Scholar
  65. 65.
    Waldrop MP, Firestone MK (2004) Altered utilization patterns of young and old soil C by microorganisms caused by temperature shifts and N additions. Biogeochemistry 67(2):235–248CrossRefGoogle Scholar
  66. 66.
    Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416(6879):389–395PubMedCrossRefGoogle Scholar
  67. 67.
    Wetzel RG, Hatcher PG, Bianchi TS (1995) Natural photolysis by ultraviolet irradiance of recalcitrant dissolved organic matter to simple substrates for rapid bacterial metabolism. Limnol Oceanogr 40(8):1369–1380CrossRefGoogle Scholar
  68. 68.
    Ylla I, Borrego C, Romaní AM, Sabater S (2009) Availability of glucose and light modulates the structure and function of a microbial biofilm. FEMS Microbiol Ecol 69(1):27–42PubMedCrossRefGoogle Scholar
  69. 69.
    Ylla I, Sanpera-Calbet I, Vázquez E, Romaní A, Muñoz I, Butturini A, Sabater S (2010) Organic matter availability during pre- and post-drought periods in a Mediterranean stream. Hydrobiologia 657:217–232CrossRefGoogle Scholar
  70. 70.
    Zoppini AM, Amalfitano S, Fazi S, Puddu A (2010) Dynamics of a benthic microbial community in a riverine environment subject to hydrological fluctuations (Mulargia River, Italy). Hydrobiologia 657:37–51CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Institute of Aquatic EcologyUniversity of GironaGironaSpain
  2. 2.Catalan Institute for Water Research (ICRA)GironaSpain

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