Biogeochemistry

, Volume 104, Issue 1–3, pp 165–181 | Cite as

Heterotrophic microbial activity in lake sediments: effects of organic electron donors

  • Isabela C. Torres
  • Kanika S. Inglett
  • K. R. Reddy
Article

Abstract

Allochthonous and autochthonous organic matter deposited in benthic sediments are mineralized by microbial communities, resulting in release of nutrients to the water column. Lakes with different trophic states may have sediments with different carbon and nutrient concentration with consequently different microbial communities. Microbial diversity of surface sediments of three subtropical lakes of different trophic state was investigated by measuring catabolic response to a wide variety of carbon-substrates. Basal carbon dioxide and methane production rates were highest in Lake Apopka (hypereutrophic), followed by Lake Annie (oligo-mesotrophic) and Lake Okeechobee (eutrophic) sediments. The oligo-mesotrophic Lake Annie showed the highest metabolic quotient (qCO2; proportion of basal respiration per unit of microbial biomass, 0.008 ± 0.001) indicating inefficient use of energy. The low qCO2 found in Lake Apopka sediment indicated higher efficiency in using energy. Lake Okeechobee sediments had intermediary values of qCO2 (M9 0.005 ± 0.001; M17 0.006 ± 0.0003; KR 0.004 ± 0.001) as compared with other lakes (lake Apopka 0.004 ± 0.14). Lake Apopka’s sediment catabolic diversity was higher than that observed in other sediments. Addition of organic electron donors to sediment samples from all lakes stimulated heterotrophic activity; however, the extent of the response varied greatly and was related to microbial biomass. The hypereutrophic Lake Apopka sediments had the highest respiration per unit of microbial biomass with the addition of electron donors indicating that these sediments respired most of the C added. These results showed that sediments with different biogeochemical properties had microbial communities with distinct catabolic responses to addition of the C sources.

Keywords

Electron donor Microbial activity Nutrients Organic carbon Sediment 

References

  1. Anderson JM (1976) An ignition method for determination of total phosphorus in lake sediments. Water Res 10:329–331CrossRefGoogle Scholar
  2. Anderson T-H (2003) Microbial eco-physiological indicators to asses soil quality. Soil Biol Biochem 98:285–293Google Scholar
  3. Anderson T-H, Domsch KH (1990) The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biol Biochem 25:393–395CrossRefGoogle Scholar
  4. Baldock JA, Masiello CA, Gélinas Y, Hedges JI (2004) Cycling and composition of organic matter in terrestrial and marine ecosystems. Mar Chem 92:39–64CrossRefGoogle Scholar
  5. Battoe LE (1985) Changes in vertical phytoplankton distribution in response to natural disturbance in a temperate and a subtropical lake. J Fresh Ecol 3:167–174CrossRefGoogle Scholar
  6. Binford MW, Brenner M (1986) Dilution of 210Pb by organic sedimentation in lakes of different trophic states, and application to studies of sediment-water interactions. Limnol Oceanog 31:584–595CrossRefGoogle Scholar
  7. Bond DR, Lovley DR (2002) Reduction of Fe(III) oxide by methanogens in the presence and absence of extracellular quinones. Environ Microbiol 4:115–124CrossRefGoogle Scholar
  8. Boström B, Andersen JM, Fleischer S, Jansson M (1988) Exchange of phosphorus across the sediment–water interface. Hydrobiologia 170:133–155CrossRefGoogle Scholar
  9. Bremer E, van Kessel C (1990) Extractability of microbial 14C and 15N following addition of variable rates of labeled glucose and (NH4)2SO4 to soil. Soil Biol Biochem 22:707–713CrossRefGoogle Scholar
  10. Capone DG, Kiene RP (1988) Comparison of microbial dynamics in marina and freshwater sediments: contrasts in anaerobic carbon catabolism. Limnol Oceanogr 33:725–749CrossRefGoogle Scholar
  11. Casper P, Chan OC, Furtado ALS, Adams DD (2003) Methane in an acidic bog lake: the influence of peat in the catchment on the biogeochemistry of methane. Aquat Sci 65:36–46CrossRefGoogle Scholar
  12. Castro H, Newman S, Reddy KR, Ogram A (2005) Distribution and stability of sulfate-reducing prokaryotic and hydrogenotrophic methanogenic assemblages in nutrient-impacted regions of the Florida Everglades. Appl Environ Microbiol 71:2695–2704CrossRefGoogle Scholar
  13. Clugston JP (1963) Lake Apopka, Florida, a changing lake and its vegetation. Q J Fla Acad Sci 26:168–174Google Scholar
  14. Conrad R (1999) Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments. FEMS Microbiol Ecol 28:193–202CrossRefGoogle Scholar
  15. Deevey ES, Binford MW, Brenner M, Whitmore TJ (1986) Sedimentary records of accelerated nutrient loading in Florida Lakes. Hydrobiologia 143:49–53CrossRefGoogle Scholar
  16. Degens BP (1998) Microbial functional diversity can be influenced by the addition of simple organic substrates to soil. Soil Biol Biochem 30:1981–1988CrossRefGoogle Scholar
  17. Degens BP, Harris JA (1997) Development of a physiological approach to measuring the catabolic diversity of soil microbial communities. Soil Biol Biochem 29:1309–1320CrossRefGoogle Scholar
  18. Degens BP, Shipper LA, Sparling GP, Vojvodic-Vukovic M (2000) Decreases in organic C reserves in soils can reduced catabolic diversity of soil microbial communities. Soil Biol Biochem 32:189–196CrossRefGoogle Scholar
  19. Engstrom DR, Schottler SP, Leavitt PR, Havens KE (2006) A reevaluation of the cultural eutrophication of Lake Okeechobee using multiproxy sediment records. Ecol Appl 16:1194–1206CrossRefGoogle Scholar
  20. EPA (1993) Methods for the determination of inorganic substances in environmental samples. Environmental Monitoring Systems Lab, Cincinnati, OHGoogle Scholar
  21. Falz KZ, Holliger C, Grobkof R, Liesack W, Nozhevnikova AN, Muller B, Wehrli B, Hahn D (1999) Vertical distribution of methanogens in the anoxic sediment of Totsee (Switzerland). Appl Environ Microbiol 65:2402–2408Google Scholar
  22. Findlay SEG, Sinsabaugh RL, Sobczack WV, Hoostal M (2003) Metabolic and structural response of hyporheic microbial communities to variation in supply of dissolved organic matter. Limnol Oceanogr 48:1608–1617CrossRefGoogle Scholar
  23. Fisher MM, Brenner M, Reddy KR (1992) A simple inexpensive, piston corer for collecting undisturbed sediment/water interface profiles. J Paleolimn 7:157–161CrossRefGoogle Scholar
  24. Fisher MM, Reddy KR, James RT (2001) Long-term changes in the sediment chemistry of a large shallow subtropical lake. J Lake Reserv Manag 17:217–232CrossRefGoogle Scholar
  25. Francaviglia R, Gataleta L, Marchionni M, Trinchera A, Aromolo R, Benedetti A, Nisini L, Morselli L, Brusori B, Olivieri P, Bernardi E (2004) Soil quality and vulnerability in a Mediterranean natural ecosystem of Central Italy. Chemosphere 55:455–466CrossRefGoogle Scholar
  26. Gale PM, Reddy KR (1994) Carbon flux between sediment and water column of a shallow subtropical, hypereutrophic lake. J Environ Qual 23:965–972CrossRefGoogle Scholar
  27. Garcia J-L, Patel BKC, Ollivier B (2000) Taxonomic, phylogenetic, and ecological diversity of methanogenic Archaea. Anaerobe 6:205–226CrossRefGoogle Scholar
  28. Glissmann K, Chin K-J, Casper P, Conrad R (2004) Methanogenic pathway and archeal community structure in the sediment of eutrophic Lake Dagow: effect of temperature. Microb Ecol 48:389–399CrossRefGoogle Scholar
  29. Gu B, Schelske CL, Brenner M (1996) Relationships between sediment and plankton isotope (δ13C and δ15N) and primary productivity in Florida lakes. Can J Fish Aquat Sci 53:875–883CrossRefGoogle Scholar
  30. Holmer M, Kristensen E (1994) Coexistence of sulfate reduction and methane production in an organic-rich sediment. Mar Ecol Prog Ser 107:177–184CrossRefGoogle Scholar
  31. Huttunen JT, Jukka A, Liikanen A, Juutinen S, Larmola T, Hammar T, Silvola J, Martikainen PJ (2003) Fluxes of methane, carbon dioxide and nitrous oxide in boreal lakes and potential anthropogenic effects on the aquatic greenhouse gas emissions. Chemosphere 52:609–621CrossRefGoogle Scholar
  32. Ivanoff DB, Reddy KR, Robinson S (1998) Chemical fractionation of organic P in histosols. Soil Sci 163:36–45CrossRefGoogle Scholar
  33. Jasson M, Bergstrom A-K, Lymer D, Vrede K, Karlsson J (2006) Bacterioplankton growth and nutrient use efficiencies under variable organic carbon and inorganic phosphorus ratios. Microb Ecol 52:358–364CrossRefGoogle Scholar
  34. Jørgensen BB (1983) Processes at the sediment water interface. In: Bolin B, Cook RB (eds) The major biogeochemical cycles and their interactions. Wiley, Chichester, pp 477–509Google Scholar
  35. King GM, Klug MJ (1982) Glucose metabolism in sediments of a eutrophic lake: tracer analysis of uptake and product formation. Appl Environ Microbiol 44:1308–1317Google Scholar
  36. Layne JN (1979) Natural features of the Lake Annie tract, Highlands County, Florida. Archbold Biological Station, FloridaGoogle Scholar
  37. Lovley DR, Klug MJ (1983) Sulfate reducers can outcompete methanogens at freshwater sulfate concentrations. Appl Environ Microbiol 45:187–192Google Scholar
  38. Lovley DR, Phillips EJP (1986) Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl Environ Microbiol 51:683–689Google Scholar
  39. Lu Y, Wassmann R, Neue HU, Huang C, Bueno CS (2000) Methanogenic responses to exogenous substrates in anaerobic soils. Soil Biol Biochem 32:1683–1690CrossRefGoogle Scholar
  40. Megonigal JP, Hines ME, Visscher PT (2004) Anaerobic Metabolism linkages to trace gases and aerobic processes. In: Schlesinger WH (ed) Biogeochemistry. Elsevier-Pergamon, Oxford, pp 317–424Google Scholar
  41. Meyers PA (1997) Organic geochemical proxies of paleoceanographic, paleolimnologic and plaeoclimatic processes. Org Geochem 27:213–250CrossRefGoogle Scholar
  42. Mulvaney RL (1996) Nitrogen-inorganic forms. In: Bigham JM (ed) Methods of soil analysis. Part 3. Chemical methods, Soil Science Society of America, Madison, WI, p 1123Google Scholar
  43. Nüsslein B, Conrad R (2000) Methane production in eutrophic Lake Plußsee: seasonal change, temperature effect and metabolic processes in the profundal sediment. Archiv für Hydrobiol 149:597–623Google Scholar
  44. Odum EP (1969) The strategy of ecosystem development. Science 164:262–270CrossRefGoogle Scholar
  45. Oreland RS (1988) Biogeochemistry of methanogenic bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. Wiley, Chichester, pp 641–705Google Scholar
  46. Phelps TJ, Zeikus JG (1984) Influence of pH on terminal carbon metabolism in anoxic sediments from a mildly acidic lake. Appl Environ Microbiol 48:1088–1095Google Scholar
  47. Reddy KR, Graetz DA (1991) Internal nutrient budget for Lake Apopka. Special Publ. SJ91-SP6. St Johns River Water Management District, Palatka, FloridaGoogle Scholar
  48. Roden EE, Wetzel RG (2003) Competition between Fe(III)-reducing and methanogenic bacteria for acetate in iron rich freshwater sediments. Microb Ecol 45:252–258CrossRefGoogle Scholar
  49. Roy R, Kluber HD, Conrad R (1997) Early initiation of methane production in anoxic rice soil despite presence of oxidants. FEMS Microb Ecol 24:311–320CrossRefGoogle Scholar
  50. Schelske CL, Coveney MF, Aldridge FJ, Kenney W, Cable JE (2000) Wind or nutrients: historical development of hypereutrophy in Lake Apopka, Florida, USA. Archiv für Hydrobiol Spec Adv Limnol 55:543–563Google Scholar
  51. Schulz S, Conrad R (1996) Influence of temperature on pathways to methane production in the permanently cold profundal sediment of Lake Constance. FEMS Microb Ecol 20:1–14CrossRefGoogle Scholar
  52. Schulz S, Matsuyama SH, Conrad R (1997) Temperature dependence of methane production from different precursors in a profundal sediment of a deep lake (Lake Constance). FEMS Microb Ecol 22:207–213CrossRefGoogle Scholar
  53. Smith EM, Prairie YT (2004) Bacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability. Limnol Oceanogr 49:137–147CrossRefGoogle Scholar
  54. Stams AJM (1994) Metabolic interactions between anaerobic bacteria in methanogenic environments. Antonie van Leeuwenhoek 66:271–294CrossRefGoogle Scholar
  55. Stouthamer AH (1976) Yield studies in microorganisms. Meadwfield Press, DurhamGoogle Scholar
  56. Suess E (1980) Particulate organic carbon flux in the ocean-surface productivity and oxygen utilization. Nature 288:260–262CrossRefGoogle Scholar
  57. Torien DF, Cavari B (1982) Effect of temperature on heterotrophic glucose uptake, mineralization and turnover rates in lake sediments. Appl Environ Microbiol 43:1–5Google Scholar
  58. Törnblon E, Rydin E (1998) Bacterial and phosphorus dynamics in profundal Lake Erken sediments following deposition of diatoms: a laboratory study. Hydrobiologia 364:55–63CrossRefGoogle Scholar
  59. Torres IC (2007) Linkage between biogeochemical properties and microbial activities in lake sediments: biotic control of organic phosphorus dynamics. Thesis, University of FloridaGoogle Scholar
  60. van Hees PAW, Jones DL, Finlay R, Godbold DL, Lundström UL (2005) The carbon we do not see—the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13CrossRefGoogle Scholar
  61. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring microbial biomass C. Soil Biol Biochem 19:703–707CrossRefGoogle Scholar
  62. Wand U, Samarkin VA, Nitzche H-M, Hubberten H-W (2006) Biogeochemistry of methane in the permanently ice-covered Lake Untersee, central Dronning Maud Land, East Antarctica. Limnol Oceanogr 51:1180–1194CrossRefGoogle Scholar
  63. Wang D, Huang Q, Wang C, Ma M, Wang Z (2007) The effects of different electron donors on anaerobic nitrogen transformations and denitrification processes in Lake Taihu sediments. Hydrobiologia 581:71–77CrossRefGoogle Scholar
  64. Wright AL, Reddy KR (2001) Heterotrophic microbial activity in northern Everglades’s wetland soils. Soil Sci Soc Am J 65:1856–1864CrossRefGoogle Scholar
  65. Wright AL, Reddy KR (2007) Substrate-induced respiration for phosphorus-enriched and oligotrophic peat soils in an Everglades Wetland. Soil Sci Soc Am J 71:1579–1583CrossRefGoogle Scholar
  66. Zinder SH (1993) Physiological ecology of methanogens. In: Ferry JG (ed) Methanogenesis: ecology, physiology, biochemistry and genetics. Chapman and Hall, New York, pp 128–206Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Isabela C. Torres
    • 1
  • Kanika S. Inglett
    • 1
  • K. R. Reddy
    • 1
  1. 1.Wetland Biogeochemistry Laboratory, Soil and Water Science DepartmentUniversity of FloridaGainesvilleUSA

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