Environmental Management

, Volume 50, Issue 5, pp 861–874 | Cite as

Relationships Between Nitrogen Transformation Rates and Gene Abundance in a Riparian Buffer Soil

  • Lin Wu
  • Deanna L. Osmond
  • Alexandria K. Graves
  • Michael R. Burchell
  • Owen W. Duckworth
Article

Abstract

Denitrification is a critical biogeochemical process that results in the conversion of nitrate to volatile products, and thus is a major route of nitrogen loss from terrestrial environments. Riparian buffers are an important management tool that is widely utilized to protect water from non-point source pollution. However, riparian buffers vary in their nitrate removal effectiveness, and thus there is a need for mechanistic studies to explore nitrate dynamics in buffer soils. The objectives of this study were to examine the influence of specific types of soluble organic matter on nitrate loss and nitrous oxide production rates, and to elucidate the relationships between these rates and the abundances of functional genes in a riparian buffer soil. Continuous-flow soil column experiments were performed to investigate the effect of three types of soluble organic matter (citric acid, alginic acid, and Suwannee River dissolved organic carbon) on rates of nitrate loss and nitrous oxide production. We found that nitrate loss rates increased as citric acid concentrations increased; however, rates of nitrate loss were weakly affected or not affected by the addition of the other types of organic matter. In all experiments, rates of nitrous oxide production mirrored nitrate loss rates. In addition, quantitative polymerase chain reaction (qPCR) was utilized to quantify the number of genes known to encode enzymes that catalyze nitrite reduction (i.e., nirS and nirK) in soil that was collected at the conclusion of column experiments. Nitrate loss and nitrous oxide production rates trended with copy numbers of both nir and 16s rDNA genes. The results suggest that low-molecular mass organic species are more effective at promoting nitrogen transformations than large biopolymers or humic substances, and also help to link genetic potential to chemical reactivity.

Keywords

Riparian buffer Nitrogen Denitrification Quantitative PCR Nitrous oxide Nitrate 

Notes

Acknowledgments

We thank Lauren Saal, Emily Dell, Guillemo Ramirez, Sara Knies, Brad Robinson, Chris Ashwell, Greg Dick, Suzanna Bräuer, Jeff White, and John Walker. This work was supported by NC Department of Environment & Natural Resources, Conservation Reserve Enhancement Program. Lin Wu thanks the Society of Wetland Scientists for a student research grant.

References

  1. Ardakani MS, Belser LW, McLaren AD (1975) Reduction of nitrate in a soil column during continuous flow. Soil Science Society of America Journal 39:290–294CrossRefGoogle Scholar
  2. Barnhill WL, Goodwin J, Bostian MR, McLoda NA, Leishman GW, Scanu RJ (1974) Soil survey of Wayne County, North Carolina. Soil Conservation Service, Washington, DCGoogle Scholar
  3. Beauchamp EG, Gale C, Yeomans JC (1980) Organic matter availability for denitrification in soils of different textures and drainage classes. Communications in Soil Science and Plant Analysis 11:1221–1233CrossRefGoogle Scholar
  4. Bernhardt ES, Likens GE (2002) Dissolved organic carbon enrichment alters nitrogen dynamics in a forest stream. Ecology 83:1689–1700CrossRefGoogle Scholar
  5. Bijay-Singh RydenJC, Whitehead DC (1988) Some relationships between denitrification potential and fractions of organic carbon in air-dried and field-moist soils. Soil Biology & Biochemistry 20:737–741CrossRefGoogle Scholar
  6. Bothe H, Jost G, Schloter M, Ward BB, Witzel KP (2000) Molecular analysis of ammonia oxidation and denitrification in natural environments. FEMS Microbiology Reviews 24:673–690CrossRefGoogle Scholar
  7. Bowman RA, Focht DD (1974) Influence of glucose and nitrate concentrations upon denitrification rates in sandy soils. Soil Biology & Biochemistry 6:297–301CrossRefGoogle Scholar
  8. Boyer JN, Groffman PM (1996) Bioavailability of water extractable organic carbon fractions in forest and agricultural soil profiles. Soil Biology & Biochemistry 28:783–790CrossRefGoogle Scholar
  9. Bradley PM, Fernandez M, Chapelle FH (1992) Carbon limitation of denitrification rates in an anaerobic groundwater system. Environmental Science and Technology 26:2377–2381CrossRefGoogle Scholar
  10. Bremner JM, Blackmer AM (1978) Nitrous oxide: emission from soils during nitrification of fertilizer nitrogen. Science 199:295–296CrossRefGoogle Scholar
  11. Burford JR, Bremner JM (1975) Relationships between denitrification capacities of soils and total, water soluble and readily decomposable soil organic-matter. Soil Biology & Biochemistry 7:389–394CrossRefGoogle Scholar
  12. Cook BD, Allan DL (1992) Dissolved organic carbon in old field soils- compositional changes during the biodegredation of soil organic-matter. Soil Biology & Biochemistry 24:595–600CrossRefGoogle Scholar
  13. Curl EA, Truelove B (1986) The rhizosphere. Springer, New YorkCrossRefGoogle Scholar
  14. Dandie CE, Burton DL, Zebarth BJ, Henderson SL, Trevors JT, Goyer C (2008) Changes in bacterial denitrifier community abundance over time in an agricultural field and their relationship with denitrification activity. Applied and Environmental Microbiology 74:5997–6005CrossRefGoogle Scholar
  15. Dandie CE, Wertz S, Leclair CL, Goyer C, Burton DL, patten CL, Zebarth BJ, Trevors JT (2011) Abundance, diversity and functional gene expression of dentrifier comminties in adjacent riparian and agricultural zones. FEMS Microbiology Ecology 77:69–82CrossRefGoogle Scholar
  16. Davidson EA, Galloway LF, Strand MK (1987) Assessing available carbon: comparison of techniques across selected forest soils. Communications in Soil Science and Plant Analysis 18:45–64CrossRefGoogle Scholar
  17. Dendooven L, Splatt P, Anderson JM (1996) Denitrification in permanent pasture soil as affected by different forms of C substrate. Soil Biology & Biochemistry 28:141–149CrossRefGoogle Scholar
  18. Dosskey MG, Vidon P, Gurwick NP, Allan CJ, Duval TP, Lowrance R (2010) The role of riparian vegetation in protecting and improving chemical water quality in streams. Journal of the American Water Resources Association 46:261–277CrossRefGoogle Scholar
  19. Drenovsky RE, Vo D, Graham KJ, Scow KM (2004) Soil water content and organic carbon availability are major determinants of soil microbial community composition. Microbial Ecology 48:424–430CrossRefGoogle Scholar
  20. Dukes MD (2000) Effect of riparian buffers and controlled drainage on shallow groundwater quality in the North Carolina Middle Coastal Plain. Doctoral Dissertation, North Carolina State University, RaleighGoogle Scholar
  21. Dukes MD, Evans RO, Gilliam JW, Kunickis SH (2002) Effect of riparian buffer width and vegetation type on shallow groundwater quality in the Middle Coastal Plain of North Carolina. Transactions of the ASAE 45:327–336Google Scholar
  22. Firestone MK, Davidson EA (1989) Microbiological basis of NO and N2O production and consumption in soil. In: Andreae MO, Schimel DS (eds) Exchange of trace gases between terrestrial ecosystems and the atmosphere, vol 47. Life Sciences Research Report. Wiley, Hoboken, NJ, pp 7–21Google Scholar
  23. Gee GW, Or D (2002) Particle-size analysis. In: Dane JH, Topp GC (eds) Methods of soil analysis. Part 4. Physical methods. Soil Science Society of America, Madison, WIGoogle Scholar
  24. Greenan CM, Moorman TB, Kaspar TC, Parkin TB, Jaynes DB (2006) Comparing carbon substrates for denitrification of subsurface drainage water. Journal of Environmental Quality 35:824–829CrossRefGoogle Scholar
  25. Groffman PM, Axelrod EA, Lemunyon JL, Sullivan WM (1991) Denitrification in grass and forest vegitated filter strips. Journal of Environmental Quality 20:671–674CrossRefGoogle Scholar
  26. Groffman PM, Gold AJ, Simmons RC (1992) Nitrate dynamics in riparian forests-microbial studies. Journal of Environmental Quality 21:666–671CrossRefGoogle Scholar
  27. Groffman PM, Altabet MA, Bohlke JK, Butterbach-Bahl K, David MB, Firestone MK, Giblin AE, Kana TM, Nielsen LP, Voytek MA (2006) Methods for measuring denitrification: diverse approaches to a difficult problem. Ecological Applications 16:2091–2122CrossRefGoogle Scholar
  28. Hedin LO, von Fischer JC, Ostrom NE, Kennedy BP, Brown MG, Robertson GP (1998) Thermodynamic constraints on nitrogen transformations and other biogeochemical processes at soil-stream interfaces. Ecology 79:684–703Google Scholar
  29. Henry S, Baudoin E, Lopez-Gutierrez JC, Martin-Laurent F, Baumann A, Philippot L (2004) Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. Journal of Microbiological Methods 59:327–335CrossRefGoogle Scholar
  30. Henry S, Texier S, Hallet S, Bru D, Dambreville C, Cheneby D, Bizouard F, Germon JC, Philippot L (2008) Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudates. Environmental Microbiology 10:3082–3092CrossRefGoogle Scholar
  31. Hernandez ME, Mitsch WJ (2007) Denitrification potential and organic matter as affected by vegetation community, wetland age, and plant introduction in created wetlands. Journal of Environmental Quality 36:333–342CrossRefGoogle Scholar
  32. Hill AR (1996) Nitrate removal in stream riparian zones. Journal of Environmental Quality 25:743–755CrossRefGoogle Scholar
  33. Hill AR, Cardaci M (2004) Denitrification and organic carbon availability in riparian wetland soils and subsurface sediments. Soil Science Society of America Journal 68:320–325CrossRefGoogle Scholar
  34. Hill AR, Devito KJ, Campagnolo S, Sanmugadas K (2000) Subsurface denitrification in a forest riparian zone: interactions between hydrology and supplies of nitrate and organic carbon. Biogeochemistry 51:193–223CrossRefGoogle Scholar
  35. Jones DL (1998) Organic acids in the rhizosphere: a critical review. Plant and Soil 205:25–44CrossRefGoogle Scholar
  36. Jones DL, Dennis PG, Owen AG, van Hees PAW (2003) Organic acid behavior in soils: misconceptions and knowledge gaps. Plant and Soil 248:31–41CrossRefGoogle Scholar
  37. Kandeler E, Deiglmayr K, Tscherko D, Bru D, Philippot L (2006) Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Applied and Environmental Microbiology 72:5957–5962CrossRefGoogle Scholar
  38. King SE (2006) Riparian buffer effectiveness in removing groundwater nitrate as influenced by vegetative type. Master’s Thesis, North Carolina State University, RaleighGoogle Scholar
  39. Knies SV (2009) Riparian buffer effectiveness at removal of NO3-N from groundwater in the middle Coastal Plain of North Carolina. Master’s Thesis, North Carolina State University, RaleighGoogle Scholar
  40. Knowles R (1982) Denitrification. Microbiological Reviews 46:43–70Google Scholar
  41. Levy-Booth DJ, Winder RS (2010) Quantification of nitrogen reductase and nitrite reductase genes in soil of thinned and clear-cut Douglas-Fir stands by using real-time PCR. Applied and Environmental Microbiology 76:7116–7125CrossRefGoogle Scholar
  42. Lowrance R (1992) Groundwater nitrate and denitrification in a coastal plain riparian forest. Journal of Environmental Quality 21:401–405CrossRefGoogle Scholar
  43. Lowrance R, Altier LS, Newbold JD, Schnabel RR, Groffman PM, Denver JM, Correll DL, Gilliam JW, Robinson JL, Brinsfield RB, Staver KW, Lucas W, Todd AH (1997) Water quality functions of riparian forest buffers in Chesapeake Bay watersheds. Environmental Management 21:687–712CrossRefGoogle Scholar
  44. Mayer PM, Reynolds SK, McCutchen MD, Canfield TJ (2007) Meta-analysis of nitrogen removal in riparian buffers. Journal of Environmental Quality 36:1172–1180CrossRefGoogle Scholar
  45. McCarty GW, Bremner JM (1992) Availability of organic carbon for denitrification of nitrate in subsoils. Biology and Fertility of Soils 14:219–222CrossRefGoogle Scholar
  46. Miller MN, Zebarth BJ, Dandie CE, Burton DL, Goyer C, Trevors JT (2009) Denitrifier community dynamics in soil aggregates under permanent grassland and arable cropping systems. Soil Science Society of America Journal 73:1843–1851CrossRefGoogle Scholar
  47. Miller MN, Dandie CE, Zebarth BJ, Burton DL, Goyer C, Trevors JT (2012) Influence of carbon amendments on soil denitrifier abundance in soil microcosms. Geoderma 170:48–55CrossRefGoogle Scholar
  48. Mounier E, Hallet S, Cheneby D, Benizri E, Gruet Y, Nguyen C, Piutti S, Robin C, Slezack-Deschaumes S, Martin-Laurent F, Germon JC, Philippot L (2004) Influence of maize mucilage on the diversity and activity of the denitrifying community. Environmental Microbiology 6:301–312CrossRefGoogle Scholar
  49. Myrold DD, Tiedje JM (1985) Establishment of denitrification capacity in soil: effects of carbon, nitrate and moisture. Soil Biology & Biochemistry 17:819–822CrossRefGoogle Scholar
  50. Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396CrossRefGoogle Scholar
  51. Nogales B, Timmis KN, Nedwell DB, Osborn AM (2002) Detection and diversity of expressed denitrification genes in estuarine sediments after reverse transcription-PCR amplification from mRNA. Applied and Environmental Microbiology 68:5017–5025CrossRefGoogle Scholar
  52. Nommik H (1956) Denitrification in soil. Acta Agriculturæ Scandinavica 6:195–228CrossRefGoogle Scholar
  53. Ocampo CJ, Oldham CE, Sivapalan M (2006) Nitrate attenuation in agricultural catchments: shifting balances between transport and reaction. Water Resources Research 42:W01408CrossRefGoogle Scholar
  54. Osborne LL, Kovacic DA (1993) Riparian vegetated buffer strips in water-quality restoration and stream management. Freshwater Biology 29:243–258CrossRefGoogle Scholar
  55. Pavel EW, Reneau RB, Berry DF, Smith EP, Mostaghimi S (1996) Denitrification potential of nontidal riparian wetland soils in the Virginia coastal plain. Water Research 30:2798–2804CrossRefGoogle Scholar
  56. Perry TD, Duckworth OW, McNamara CJ, Martin ST, Mitchell R (2004) The effects of the biologically produced polymer alginic acid on macroscopic and microscopic calcite dissolution rates. Environmental Science and Technology 38:3040–3046CrossRefGoogle Scholar
  57. Perry TD, Cygan RT, Mitchell R (2006) Molecular models of alginic acid: interactions with calcium ions and calcite surfaces. Geochimica et Cosmochimica Acta 70:3508–3532CrossRefGoogle Scholar
  58. Philippot L (2002) Denitrifying genes in bacterial and archaeal genomes. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression 1577:355–376CrossRefGoogle Scholar
  59. Philippot L, Hallin S, Schloter M (2007) Ecology of denitrifying prokaryotes in agricultural soil. Advances in Agronomy 96:249–305CrossRefGoogle Scholar
  60. Pintar M, Lobnik F (2005) The impact of nitrate and glucose availability on the denitrification at different soil depths. Fresenius Environmental Bulletin 14:514–519Google Scholar
  61. Rivett MO, Buss SR, Morgan P, Smith JWN, Bemment CD (2008) Nitrate attenuation in groundwater: a review of biogeochemical controlling processes. Water Research 42:4215–4232CrossRefGoogle Scholar
  62. Sirivedhin T, Gray KA (2006) Factors affecting denitrification rates in experimental wetlands: field and laboratory studies. Ecological Engineering 26:167–181CrossRefGoogle Scholar
  63. Smith TA, Osmond DL, Gilliam JW (2006) Riparian buffer width and nitrate removal in a lagoon-effluent irrigated agricuttural area. Journal of Soil and Water Conservation 61:273–281Google Scholar
  64. Stanford G, Vanderpol RA, Dzienia S (1975) Denitrification rates in relation to total and extractable soil carbon. Soil Science Society of America Journal 39:284–289CrossRefGoogle Scholar
  65. Starr RC, Gillham RW (1993) Denitrification and organic carbon availability in two aquifers. Ground Water 31:934–947CrossRefGoogle Scholar
  66. Stow CA, Walker JT, Cardoch L, Spence P, Stow CA (2005) N2O emissions from streams in the Neuse River watershed, North Carolina. Environmental Science and Technology 39:6999–7004CrossRefGoogle Scholar
  67. Stumm W, Morgan JJ (1996) Aquatic chemistry, 3rd edn. Wiley, New YorkGoogle Scholar
  68. Tate RL (1987) Soil organic matter: biological and ecological effects. Wiley, New YorkGoogle Scholar
  69. Throback IN, Enwall K, Jarvis A, Hallin S (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiology Ecology 49:401–417CrossRefGoogle Scholar
  70. Thurman EM (1985) Organic geochemistry of natural waters. Kluwer, BostonCrossRefGoogle Scholar
  71. van Hees PAW, Jones DL, Finlay R, Godbold DL, Lundstom US (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 Biology & Biochemistry 37:1–13CrossRefGoogle Scholar
  72. Van Mooy BAS, Keil RG, Devol AH (2002) Impact of suboxia on sinking particulate organic carbon: enhanced carbon flux and preferential degradation of amino acids via denitrification. Geochimica et Cosmochimica Acta 66:457–465CrossRefGoogle Scholar
  73. Wallenstein MD, Myrold DD, Firestone M, Voytek M (2006) Environmental controls on denitrifying communities and denitrification rates: insights from molecular methods. Ecological Applications 16:2143–2152CrossRefGoogle Scholar
  74. Ward BB, Devol AH, Rich JJ, Chang BX, Bulow SE, Naik H, Pratihary A, Jayakumar A (2009) Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature 461:78–81CrossRefGoogle Scholar
  75. Willems HPL, Rotelli MD, Berry DF, Smith EP, Reneau RB, Mostaghimi S (1997) Nitrate removal in riparian wetland soils: effects of flow rate, temperature, nitrate concentration and soil depth. Water Research 31:841–849CrossRefGoogle Scholar
  76. Yoshida M, Ishii S, Otsuka S, Senoo K (2009) Temporal shifts in diversity and quantity of nirS and nirK in a rice paddy field soil. Soil Biology & Biochemistry 41:2044–2051CrossRefGoogle Scholar
  77. Yoshida M, Ishii S, Otsuka S, Senoo K (2010) nirK-harboring denitrifiers are more responsive to denitrification inducing conditions in rice paddy soil than nirS-harboring bacteria. Microbes and Environments 25:45–48CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Lin Wu
    • 1
    • 3
  • Deanna L. Osmond
    • 1
  • Alexandria K. Graves
    • 1
  • Michael R. Burchell
    • 2
  • Owen W. Duckworth
    • 1
  1. 1.Department of Soil ScienceNorth Carolina State UniversityRaleighUSA
  2. 2.Department of Biological and Agricultural EngineeringNorth Carolina State UniversityRaleighUSA
  3. 3.Department of StatisticsUniversity of North CarolinaChapel HillUSA

Personalised recommendations