Skip to main content

Advertisement

SpringerLink
Log in

Resource Availability Effects on Nitrate-Reducing Microbial Communities in a Freshwater Wetland

  • Article
  • Published:
Wetlands Aims and scope Submit manuscript

Abstract

Microbial communities in freshwater wetland soils process nitrate via denitrification (DNF) and dissimilatory nitrate reduction to ammonium (DNRA). Because the processes generate different end products (N-gas versus NH4 +), the relative dominance of DNF versus DNRA has implications for ecosystem nitrogen cycling, greenhouse gas production, and downstream eutrophication. To examine how resource availability affects these two microbial groups, wetland soil was supplemented with labile (compost) or recalcitrant (wood) organic matter (OM) and/or potassium nitrate fertilizer. Following a three-month in situ incubation, the abundance and composition of the DNF- and DNRA-capable microbes were examined via quantitative polymerase chain reaction (qPCR) and terminal restriction fragment length polymorphism (T-RFLP) using process-specific functional genes (DNF: nirS qPCR, nosZ T-RFLP; DNRA: nrfA qPCR and T-RFLP). Denitrifer abundance was positively related to OM lability and simultaneous nitrate amendment enhanced OM effects, while DNRA abundance varied little across treatments. For both groups, community structure showed an interactive response to OM type and nitrate availability, even when abundances did not change. This work highlights the importance of considering co-varying resource gradients, and the differential responses of DNF and DNRA communities to resource manipulation provides insight into the environmental regulators of ecosystem nitrate removal in wetlands.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences USA 105:11512–11519

    Article  CAS  Google Scholar 

  • An S, Gardner W (2002) Dissimilatory nitrate reduction to ammonium (DNRA) as a nitrogen link, versus denitrification as a sink in a shallow estuary (Laguna Madre/Baffin Bay, Texas). Marine Ecology Progress Series 237:41–50

    Article  CAS  Google Scholar 

  • Antil RS, Bar Tal A, Fine P, Hadas A (2011) Predicting nitrogen and carbon mineralization of composted manure and sewage sludge in soil. Compost Science Utilization 19:33–43

    CAS  Google Scholar 

  • Attard E, Recous S, Chabbi A, De Berranger C, Guillaumaud N, Labreuche J, Philippot L, Schmid B, Roux L (2011) Soil environmental conditions rather than denitrifier abundance and diversity drive potential denitrification after changes in land uses. Global Change Biology 17:1975–1989

    Article  Google Scholar 

  • Baxter A, Johnson L, Edgerton J, Royer T, Leff L (2012) Structure and function of denitrifying bacterial assemblages in low-order Indiana streams. Freshwater Science 31:304–317

    Article  Google Scholar 

  • Bruland GL, Richardson CJ, Daniels WL (2009) Microbial and geochemical responses to organic matter amendments in a created wetland. Wetlands 29:1153–1165

    Article  Google Scholar 

  • Burchell MR II, Skaggs RW, Lee CR, Broome S, Chescheir GM, Osborne J (2007) Substrate organic matter to improve nitrate removal in surface-flow constructed wetlands. Journal of Environmental Quality 36:194–207

    Article  PubMed  CAS  Google Scholar 

  • Burgin A, Hamilton S (2007) Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Frontiers in Ecology and the Environment 5:89–96

    Article  Google Scholar 

  • Button D (1993) Nutrient-limited microbial growth kinetics: overview and recent advances. Anton Van Leeuwenhoek 63:225–235

    Article  CAS  Google Scholar 

  • Canfield D, Glazer A, Falkowski P (2010) The evolution and future of Earth’s nitrogen cycle. Science 330:192–196

    Article  PubMed  CAS  Google Scholar 

  • Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiology Reviews 60:609–640

    CAS  Google Scholar 

  • Dang H, Wang C, Li J, Li T, Tian F, Jin W, Ding Y, Zhang Z (2009) Diversity and distribution of sediment nirS-encoding bacterial assemblages in response to environmental gradients in the eutrophiedJiaozhou Bay, China. Microbial Ecology 58:161–169

    Article  PubMed  CAS  Google Scholar 

  • Davis L (1995) A handbook of constructed wetlands: A guide to creating wetlands for-agricultural wastewater, domestic wastewater, coal mine drainage, stormwater in the Mid-Atlantic Region. USDA-Natural Resources Conservation Service and the US Environmental Protection Agency, 55 pp

  • Dimitriu P, Lee D, Grayston S (2010) An evaluation of the functional significance of peat microorganisms using a reciprocal transplant approach. Soil Biology and Biochemistry 42:65–71

    Article  CAS  Google Scholar 

  • Dodla S, Wang J, DeLaune R, Cook R (2008) Denitrification potential and its relation to organic carbon quality in three coastal wetland soils. Science of the Total Environment 407:471–480

    Article  PubMed  CAS  Google Scholar 

  • Doutereol I, Goulder R, Lillie M (2010) Soil microbial community response to land-management and depth, related to the degradation of organic matter in English wetlands: Implications for the in situ preservation of archaeological remains. Applied Soil Ecology 44:219–227

    Article  Google Scholar 

  • Erler DV, Eyre BD, Davison L (2008) The contribution of anammox and denitrification to sediment N2 production in a surface flow constructed wetland. Environmental Science and Technology 42:9144–9150

    Article  PubMed  CAS  Google Scholar 

  • Fierer N, Bradford M, Jackson R (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  PubMed  Google Scholar 

  • Fisher J, Acreman M (2004) Wetland nutrient removal: a review of the evidence. Hydrology and Earth System Science 8:673–685

    Article  CAS  Google Scholar 

  • Fleming-Singer MS, Horne AJ (2002) Enhanced nitrate removal efficiency in wetland microcosms using an episediment layer for denitrification. Environmental Science and Technology 36:1231–1237

    Article  PubMed  CAS  Google Scholar 

  • Fuhrman J (2009) Microbial community structure and its functional implications. Nature 459:193–199

    Article  PubMed  CAS  Google Scholar 

  • Hammer Ø (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Hill A, Cardaci M (2004) Denitrification and organic carbon availability in riparian wetland soils and subsurface sediments. Soil Science Society of America Journal 68:320–325

    Article  CAS  Google Scholar 

  • Jones C, Hallin S (2010) Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME Journal 4:633–642

    Article  PubMed  Google Scholar 

  • Jones C, Stres B, Rosenquist M, Hallin S (2008) Phylogenetic analysis of nitrite, nitric oxide, and nitrous oxide respiratory enzymes reveal a complex evolutionary history for denitrification. Molecular Biology and Evolution 25:1955–1966

    Article  PubMed  CAS  Google Scholar 

  • Kadlec R (2012) Constructed marshes for nitrate removal. Critical Reviews in Environmental Science and Technology 42:934–1005

    Article  CAS  Google Scholar 

  • Kiesel B, Balcke G, Dietrich J, Vogt C, Geyer R (2008) Microbial community shifts as a response to efficient degradation of chlorobenzene under hypoxic conditions. Biodegradation 19:435–446

    Article  PubMed  CAS  Google Scholar 

  • Koop-Jakobsen K, Giblin A (2009) Anammox in tidal marsh sediments: the role of salinity, nitrogen loading, and marsh vegetation. Estuaries and Coasts 32:238–245

    Article  CAS  Google Scholar 

  • Koop-Jakobsen K, Giblin A (2010) The effect of increased nitrate loading on nitrate reduction via denitrification and DNRA in salt marsh sediments. Limnology and Oceanography 55:789–802

    Article  CAS  Google Scholar 

  • Kovárová-Kovar K, Egli T (1998) Growth kinetics of suspended microbial cells: From single-substrate-controlled growth to mixed-substrate kinetics. Microbiology and Molecular Biology Reviews 62:646–666

    PubMed  Google Scholar 

  • Krishnani K (2010) Detection and diversity of nitrifying and denitrifying functional genes in coastal aquaculture. Aquaculture 302:57–70

    Article  CAS  Google Scholar 

  • Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, Gutierrez D, Amann R, Jetten MS, Kuypers MM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proceedings of the National Academy of Sciences USA 106:4752–4757

    Article  CAS  Google Scholar 

  • Lou Y, Ren L, Li Z, Zhang T, Inubushi K (2007) Effect of rice residues on carbon dioxide and nitrous oxide emissions from a paddy soil of subtropical China. Water Air and Soil Pollution 178:157–168

    Article  CAS  Google Scholar 

  • Ma H, Aelion C (2005) Ammonium production during microbial nitrate removal in soil microcosms from a developing marsh estuary. Soil Biology and Biochemistry 37:1869–1878

    Article  CAS  Google Scholar 

  • Magalhaes C, Bano N, Wiebe W, Bordalo A, Hollibaugh J (2008) Dynamics of nitrous oxide reductase genes (nosZ) in intertidal rocky biofilms and sediments of the Douro River Estuary (Portugal), and their relation to N-biogeochemistry. Microbial Ecology 55:259–269

    Article  PubMed  CAS  Google Scholar 

  • Mohan S, Schmid M, Jetten M, Cole J (2004) Detection and widespread distribution of the nrfAgene encoding nitrite reduction to ammonia, a short circuit in the biological nitrogen cycle that competes with denitrification. FEMS Microbiology Ecology 49:433–443

    Article  PubMed  CAS  Google Scholar 

  • Moore T, Trofymow J, Siltanen M, Prescott C (2005) Patterns of decomposition and carbon, nitrogen, and phosphorus dynamics of litter in upland forest and peatland sites in central Canada. Canadian Journal of Forest Research 35:133–142

    Article  CAS  Google Scholar 

  • Nizzoli D, Carraro E, Nigro V, Viaroli P (2010) Effect of organic enrichment and thermal regime on denitrification and dissimilatory nitrate reduction to ammonium (DNRA) in hypolimnetic sediments of two lowland lakes. Water Research 44:2715–2724

    Article  PubMed  CAS  Google Scholar 

  • Oksanen JF, Blanchet G, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos PM, Stevens HH, Wagner H (2012) vegan: Community Ecology Package. R package version 2.0–3

  • Peralta A, Matthews J, Kent A (2010) Microbial community structure and denitrification in a wetland mitigation bank. Applied and Environmental Microbiology 76:4207–4215

    Article  PubMed  CAS  Google Scholar 

  • Philippot L, Hallin S (2005) Finding the missing link between diversity and activity using denitrifying bacteria as a model functional community. Current Opinions in Microbiology 8:234–239

    Article  CAS  Google Scholar 

  • Reddy R, DeLaune R (2008) Biogeochemistry of wetlands: science and applications. CRC Press Taylor and Francis Group, Boca Raton

    Book  Google Scholar 

  • Reed H, Martiny J (2007) Testing the functional significance of microbial composition in natural communities. FEMS Microbiology Ecology 62:161–170

    Article  PubMed  CAS  Google Scholar 

  • Sall J (2005) JMP start statistics: a guide to statistics and data analysis using JMP and JMP IN software. SAS Institute Inc, Cary

    Google Scholar 

  • Scott J, McCarthy M, Gardner W, Doyle R (2008) Denitrification, dissimilatory nitrate reduction to ammonium, and nitrogen fixation along a nitrate concentration gradient in a created freshwater wetland. Biogeochemistry 87:99–111

    Article  CAS  Google Scholar 

  • Smith C, Nedwell D, Dong L, Osborn AM (2007) Diversity and abundance of nitrate reductase genes (narGand napA), nitrite reductase genes (nirS and nrfA), and their transcripts in estuarine sediments. Applied and Environmental Microbiology 73:3612–3622

    Article  PubMed  CAS  Google Scholar 

  • Song K, Lee S, Kang H (2011) Denitrification rates and community structure of denitrifying bacteria in newly constructed wetland. European Journal of Soil Biology 47:24–29

    Article  CAS  Google Scholar 

  • Sutton-Grier A, Ho M, Richardson C (2009) Organic amendments improve soil conditions and denitrification in a restored riparian wetland. Wetlands 29:343–352

    Article  Google Scholar 

  • Takeuchi J (2006) Habitat segregation of a functional gene encoding nitrate ammonification in estuarine sediments. Geomicrobiology Journal 23:75–87

    Article  CAS  Google Scholar 

  • Tang H, Yan K, Zhang L, Chi F, Li Q, Lian S, Wei D (2010) Diversity analysis of nitrite reductase genes (nirS) in black soil under different long-term fertilization conditions. Annals of Microbiology 60:97–104

    Article  CAS  Google Scholar 

  • Throback I, 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 49:401–417

    Article  PubMed  CAS  Google Scholar 

  • Thullner M, Regnier P, Van Cappellen P (2007) Modeling microbially-induced carbon degradation in redox-stratified subsurface environments: Concepts and open questions. Geomicrobiology Journal 24:139–155

    Article  CAS  Google Scholar 

  • Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder A (ed) Biology of anaerobic microorganisms. John Wiley and Sons, New York, pp 179–244

    Google Scholar 

  • Tuomela M, Vikman M, Hatakka A, Itävaara M (2000) Biodegradation of lignin in a compost environment: a review. Bioresource Technology 72:169–183

    Article  CAS  Google Scholar 

  • Ullah S, Faulkner S (2006) Use of cotton gin trash to enhance denitrification in restored forested wetlands. Forest Ecology and Management 237:557–563

    Article  Google Scholar 

  • Warneke S, Schipper L, Matiasek M, Scow K, Cameron S, Bruesewitz D, McDonald I (2011) Nitrate removal, communities of denitrifiers and adverse effects in different carbon substrates for use in denitrification beds. Water Research 45:5463–5475

    Article  PubMed  CAS  Google Scholar 

  • Wolsing M, Prieme A (2004) Observation of high seasonal variation in community structure of denitrifying bacteria in arable soil receiving artificial fertilizer and cattle manure by determining T-RFLP of nir gene fragments. FEMS Microbiology Ecology 48:261–271

    Article  PubMed  CAS  Google Scholar 

  • Yadav S, Kaushik R, Saxena A, Arora D (2011) Diversity and phylogeny of plant growth-promoting bacilli from moderately acidic soil. Journal of Basic Microbiology 51:98–106

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was funded by a Virginia Commonwealth University Rice Center for the Environmental Sciences Student Research Award to E.M. Morrissey and A.S. Jenkins. We are grateful to the following people for field and laboratory help: David Berrier, Jaimie Gillespie, RanaMehr, Caitlin Muse, Aaron Aunins, and Colleen Higgins. This paper is VCU Rice Center Research Contribution No. 30.

Author information

Authors and Affiliations

  1. Department of Biology, Virginia Commonwealth University, 1000 W Cary Street, Richmond, VA, 23284, USA

    Ember M. Morrissey, Amy S. Jenkins, Bonnie L. Brown & Rima B. Franklin

  2. VCU Department of Biology, Laboratory of Microbial Ecology, 1000 W Cary Street, Richmond, VA, 23284, USA

    Rima B. Franklin

Authors
  1. Ember M. Morrissey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amy S. Jenkins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bonnie L. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rima B. Franklin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rima B. Franklin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morrissey, E.M., Jenkins, A.S., Brown, B.L. et al. Resource Availability Effects on Nitrate-Reducing Microbial Communities in a Freshwater Wetland. Wetlands 33, 301–310 (2013). https://doi.org/10.1007/s13157-013-0384-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13157-013-0384-2

Keywords

Search

Navigation