Restoring wetlands on intensive agricultural lands modifies nitrogen cycling microbial communities and reduces N2O production potential
Abstract
The concentration of nitrous oxide (N2O), an ozone-depleting greenhouse gas, is rapidly increasing in the atmosphere. Most atmospheric N2O originates in terrestrial ecosystems, of which the majority can be attributed to microbial cycling of nitrogen in agricultural soils. Here, in this study, we demonstrate how the abundance of nitrogen cycling genes vary across intensively managed agricultural fields and adjacent restored wetlands in the Sacramento-San Joaquin Delta in California, USA. We found that the abundances of nirS and nirK genes were highest at the intensively managed organic-rich cornfield and significantly outnumber any other gene abundances, suggesting very high N2O production potential. The quantity of nitrogen transforming genes, particularly those responsible for denitrification, nitrification and DNRA, were highest in the agricultural sites, whereas nitrogen fixation and ANAMMOX was strongly associated with the wetland sites. Although the abundance of nosZ genes was also high at the agricultural sites, the ratio of nosZ genes to nir genes was significantly higher in wetland sites indicating that these sites could act as a sink of N2O. These findings suggest that wetland restoration could be a promising natural climate solution not only for carbon sequestration but also for reduced N2O emissions.
- Authors:
-
[1];
[1];
[2];
[3];
[5];
[1];
[2];
[2];
- University of Tartu (Estonia)
- Univ. of California, Berkeley, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Agroscope (Switzerland)
- Stanford Univ., CA (United States)
- Univ. of Illinois, Chicago, IL (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA; Estonian Research Council; European Union (EU)
- OSTI Identifier:
- 1902116
- Grant/Contract Number:
- AC02-05CH11231; 7079856; 2011-67003-30371; PSG631; PRG352; MOBERC20
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Environmental Management
- Additional Journal Information:
- Journal Volume: 299; Journal ID: ISSN 0301-4797
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Functional genes; Land use change; Land management; Nitrogen fixation; Denitrification; Ammonia oxidation
Citation Formats
Kasak, Kuno, Espenberg, Mikk, Anthony, Tyler L., Tringe, Susannah G., Valach, Alex C., Hemes, Kyle S., Silver, Whendee L., Mander, Ülo, Kill, Keit, McNicol, Gavin, Szutu, Daphne, Verfaillie, Joseph, and Baldocchi, Dennis D. Restoring wetlands on intensive agricultural lands modifies nitrogen cycling microbial communities and reduces N2O production potential. United States: N. p., 2021.
Web. doi:10.1016/j.jenvman.2021.113562.
Kasak, Kuno, Espenberg, Mikk, Anthony, Tyler L., Tringe, Susannah G., Valach, Alex C., Hemes, Kyle S., Silver, Whendee L., Mander, Ülo, Kill, Keit, McNicol, Gavin, Szutu, Daphne, Verfaillie, Joseph, & Baldocchi, Dennis D. Restoring wetlands on intensive agricultural lands modifies nitrogen cycling microbial communities and reduces N2O production potential. United States. https://doi.org/10.1016/j.jenvman.2021.113562
Kasak, Kuno, Espenberg, Mikk, Anthony, Tyler L., Tringe, Susannah G., Valach, Alex C., Hemes, Kyle S., Silver, Whendee L., Mander, Ülo, Kill, Keit, McNicol, Gavin, Szutu, Daphne, Verfaillie, Joseph, and Baldocchi, Dennis D. Fri .
"Restoring wetlands on intensive agricultural lands modifies nitrogen cycling microbial communities and reduces N2O production potential". United States. https://doi.org/10.1016/j.jenvman.2021.113562. https://www.osti.gov/servlets/purl/1902116.
@article{osti_1902116,
title = {Restoring wetlands on intensive agricultural lands modifies nitrogen cycling microbial communities and reduces N2O production potential},
author = {Kasak, Kuno and Espenberg, Mikk and Anthony, Tyler L. and Tringe, Susannah G. and Valach, Alex C. and Hemes, Kyle S. and Silver, Whendee L. and Mander, Ülo and Kill, Keit and McNicol, Gavin and Szutu, Daphne and Verfaillie, Joseph and Baldocchi, Dennis D.},
abstractNote = {The concentration of nitrous oxide (N2O), an ozone-depleting greenhouse gas, is rapidly increasing in the atmosphere. Most atmospheric N2O originates in terrestrial ecosystems, of which the majority can be attributed to microbial cycling of nitrogen in agricultural soils. Here, in this study, we demonstrate how the abundance of nitrogen cycling genes vary across intensively managed agricultural fields and adjacent restored wetlands in the Sacramento-San Joaquin Delta in California, USA. We found that the abundances of nirS and nirK genes were highest at the intensively managed organic-rich cornfield and significantly outnumber any other gene abundances, suggesting very high N2O production potential. The quantity of nitrogen transforming genes, particularly those responsible for denitrification, nitrification and DNRA, were highest in the agricultural sites, whereas nitrogen fixation and ANAMMOX was strongly associated with the wetland sites. Although the abundance of nosZ genes was also high at the agricultural sites, the ratio of nosZ genes to nir genes was significantly higher in wetland sites indicating that these sites could act as a sink of N2O. These findings suggest that wetland restoration could be a promising natural climate solution not only for carbon sequestration but also for reduced N2O emissions.},
doi = {10.1016/j.jenvman.2021.113562},
journal = {Journal of Environmental Management},
number = ,
volume = 299,
place = {United States},
year = {Fri Aug 20 00:00:00 EDT 2021},
month = {Fri Aug 20 00:00:00 EDT 2021}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Plant community, primary productivity, and environmental conditions following wetland re-establishment in the Sacramento-San Joaquin Delta, California
journal, May 2009
- Miller, Robin L.; Fujii, Roger
- Wetlands Ecology and Management, Vol. 18, Issue 1
Proteomic analysis of the cyanobacterium of the Azolla symbiosis: identity, adaptation, and NifH modification
journal, February 2008
- Ekman, M.; Tollback, P.; Bergman, B.
- Journal of Experimental Botany, Vol. 59, Issue 5
Soil CN ratio as a scalar parameter to predict nitrous oxide emissions
journal, July 2005
- Klemedtsson, Leif; Von Arnold, Karin; Weslien, Per
- Global Change Biology, Vol. 11, Issue 7
Nitrate Runoff Contributing from the Agriculturally Intensive San Joaquin River Watershed to Bay-Delta in California
journal, May 2019
- Wang, Ruoyu; Chen, Huajin; Luo, Yuzhou
- Sustainability, Vol. 11, Issue 10
Effects of soil Acidity on Rhizobia Numbers, Nodulation and Nitrogen Fixation by Alfalfa and red Clover
journal, May 1977
- Rice, W. A.; Penney, D. C.; Nyborg, M.
- Canadian Journal of Soil Science, Vol. 57, Issue 2
Recently identified microbial guild mediates soil N2O sink capacity
journal, July 2014
- Jones, Christopher M.; Spor, Ayme; Brennan, Fiona P.
- Nature Climate Change, Vol. 4, Issue 9
RETRACTED ARTICLE: Archaeal amoA Genes Outnumber Bacterial amoA Genes in Municipal Wastewater Treatment Plants in Bangkok
journal, June 2011
- Kayee, Pantip; Sonthiphand, Puntipar; Rongsayamanont, Chaiwat
- Microbial Ecology, Vol. 62, Issue 4
The ade4 Package: Implementing the Duality Diagram for Ecologists
journal, January 2007
- Dray, Stéphane; Dufour, Anne-Béatrice
- Journal of Statistical Software, Vol. 22, Issue 4
Separate effects of flooding and anaerobiosis on soil greenhouse gas emissions and redox sensitive biogeochemistry: Separate flooding effects on soil fluxes
journal, April 2014
- McNicol, Gavin; Silver, Whendee L.
- Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 4
Soil mineralogy trends in California landscapes
journal, January 2010
- Graham, R. C.; O'Geen, A. T.
- Geoderma, Vol. 154, Issue 3-4
Nitrogen-rich organic soils under warm well-drained conditions are global nitrous oxide emission hotspots
journal, March 2018
- Pärn, Jaan; Verhoeven, Jos T. A.; Butterbach-Bahl, Klaus
- Nature Communications, Vol. 9, Issue 1
Ammonia oxidation coupled to CO2 fixation by archaea and bacteria in an agricultural soil
journal, February 2011
- Pratscher, J.; Dumont, M. G.; Conrad, R.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 10
Differences in microbial community structure and nitrogen cycling in natural and drained tropical peatland soils
journal, March 2018
- Espenberg, Mikk; Truu, Marika; Mander, Ülo
- Scientific Reports, Vol. 8, Issue 1
Dissimilatory nitrate reduction to ammonium (DNRA), not denitrification dominates nitrate reduction in subtropical pasture soils upon rewetting
journal, October 2018
- Friedl, Johannes; De Rosa, Daniele; Rowlings, David W.
- Soil Biology and Biochemistry, Vol. 125
Spatial and temporal dynamics of nitrogen fixing, nitrifying and denitrifying microbes in an unfertilized grassland soil
journal, June 2017
- Regan, Kathleen; Stempfhuber, Barbara; Schloter, Michael
- Soil Biology and Biochemistry, Vol. 109
Assessing the carbon and climate benefit of restoring degraded agricultural peat soils to managed wetlands
journal, April 2019
- Hemes, Kyle S.; Chamberlain, Samuel D.; Eichelmann, Elke
- Agricultural and Forest Meteorology, Vol. 268
A Biogeochemical Compromise: The High Methane Cost of Sequestering Carbon in Restored Wetlands
journal, June 2018
- Hemes, Kyle S.; Chamberlain, Samuel D.; Eichelmann, Elke
- Geophysical Research Letters, Vol. 45, Issue 12
Co-Occurring Anammox, Denitrification, and Codenitrification in Agricultural Soils
journal, October 2012
- Long, Andrew; Heitman, Joshua; Tobias, Craig
- Applied and Environmental Microbiology, Vol. 79, Issue 1
Dissimilatory nitrate reduction to ammonium coupled to Fe(II) oxidation in sediments of a periodically hypoxic estuary
journal, October 2015
- Robertson, Elizabeth K.; Roberts, Keryn L.; Burdorf, Laurine D. W.
- Limnology and Oceanography, Vol. 61, Issue 1
Processes of soil acidification during nitrogen cycling with emphasis on legume based pastures
journal, July 1991
- Bolan, N. S.; Hedley, M. J.; White, R. E.
- Plant and Soil, Vol. 134, Issue 1
The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink
journal, November 2012
- Jones, Christopher M.; Graf, Daniel RH; Bru, David
- The ISME Journal, Vol. 7, Issue 2
Productive wetlands restored for carbon sequestration quickly become net CO2 sinks with site-level factors driving uptake variability
journal, March 2021
- Valach, Alex C.; Kasak, Kuno; Hemes, Kyle S.
- PLOS ONE, Vol. 16, Issue 3
Nitrous oxide production and consumption: regulation of gene expression by gas-sensitive transcription factors
journal, May 2012
- Spiro, Stephen
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1593
Nitrous oxide fluxes determined by continuous eddy covariance measurements from intensively grazed pastures: Temporal patterns and environmental controls
journal, December 2018
- Liang, Liyin L.; Campbell, David I.; Wall, Aaron M.
- Agriculture, Ecosystems & Environment, Vol. 268
Effect of pH, temperature and substrate on N2O, NO and CO2 production by Alcaligenes faecalis p.
journal, September 2006
- Kesik, M.; Blagodatsky, S.; Papen, H.
- Journal of Applied Microbiology, Vol. 101, Issue 3
Linking Annual N2O Emission in Organic Soils to Mineral Nitrogen Input as Estimated by Heterotrophic Respiration and Soil C/N Ratio
journal, May 2014
- Mu, Zhijian; Huang, Aiying; Ni, Jiupai
- PLoS ONE, Vol. 9, Issue 5
Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data
journal, February 2009
- Ruijter, J. M.; Ramakers, C.; Hoogaars, W. M. H.
- Nucleic Acids Research, Vol. 37, Issue 6
Large Greenhouse Gas Emissions from a Temperate Peatland Pasture
journal, February 2011
- Teh, Yit Arn; Silver, Whendee L.; Sonnentag, Oliver
- Ecosystems, Vol. 14, Issue 2
Effect of pH and Temperature on Denitrification Gene Expression and Activity in Pseudomonas mandelii
journal, June 2009
- Saleh-Lakha, Saleema; Shannon, Kelly E.; Henderson, Sherri L.
- Applied and Environmental Microbiology, Vol. 75, Issue 12
A comprehensive quantification of global nitrous oxide sources and sinks
journal, October 2020
- Tian, Hanqin; Xu, Rongting; Canadell, Josep G.
- Nature, Vol. 586, Issue 7828
Changing pH shifts the microbial sourceas well as the magnitude of N2O emission from soil
journal, July 2010
- Baggs, Elizabeth M.; Smales, Claire L.; Bateman, Emma J.
- Biology and Fertility of Soils, Vol. 46, Issue 8
The influence of soil pH on denitrification: progress towards the understanding of this interaction over the last 50 years
journal, September 2002
- SImek, M.; Cooper, J. E.
- European Journal of Soil Science, Vol. 53, Issue 3
Trends and seasonal cycles in the isotopic composition of nitrous oxide since 1940
journal, March 2012
- Park, S.; Croteau, P.; Boering, K. A.
- Nature Geoscience, Vol. 5, Issue 4
Soil properties and sediment accretion modulate methane fluxes from restored wetlands
journal, April 2018
- Chamberlain, Samuel D.; Anthony, Tyler L.; Silver, Whendee L.
- Global Change Biology, Vol. 24, Issue 9
Nitrous Oxide from Soil Denitrification: Factors Controlling Its Biological Production
journal, May 1980
- Firestone, M. K.; Firestone, R. B.; Tiedje, J. M.
- Science, Vol. 208, Issue 4445
A modified single solution method for the determination of phosphate in natural waters
journal, January 1962
- Murphy, J.; Riley, J. P.
- Analytica Chimica Acta, Vol. 27
Abundance of anammox bacteria in different wetland soils
journal, May 2012
- Humbert, Sylvia; Zopfi, Jakob; Tarnawski, Sonia-Estelle
- Environmental Microbiology Reports, Vol. 4, Issue 5
A Unique Combination of Aerodynamic and Surface Properties Contribute to Surface Cooling in Restored Wetlands of the Sacramento‐San Joaquin Delta, California
journal, July 2018
- Hemes, Kyle S.; Eichelmann, Elke; Chamberlain, Samuel D.
- Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 7
Adaptation to Temperature of Nitric Oxide-Producing Nitrate-Reducing Bacterial Populations in Soil
journal, April 1993
- Saad, Omar A. L. O.; Conrad, Ralf
- Systematic and Applied Microbiology, Vol. 16, Issue 1
Temporal variation in the biomass and nutrient status of Azolla filiculoides Lam. (Salviniaceae) in a small shallow dystrophic lake
journal, May 2012
- Trindade, Claudio Rossano Trindade; Albertoni, Edélti Faria; Palma-Silva, Cleber
- Acta Limnologica Brasiliensia, Vol. 23, Issue 4
Evaluation of activity and inhibition effects on Anammox process by batch tests based on the nitrogen gas production
journal, March 2007
- Dapena-Mora, A.; Fernández, I.; Campos, J. L.
- Enzyme and Microbial Technology, Vol. 40, Issue 4
Soil Bacterial and Archaeal Communities and Their Potential to Perform N-Cycling Processes in Soils of Boreal Forests Growing on Well-Drained Peat
journal, December 2020
- Truu, Marika; Nõlvak, Hiie; Ostonen, Ivika
- Frontiers in Microbiology, Vol. 11
Hot moments drive extreme nitrous oxide and methane emissions from agricultural peatlands
journal, July 2021
- Anthony, Tyler L.; Silver, Whendee L.
- Global Change Biology, Vol. 27, Issue 20
Community-specific pH response of denitrification: experiments with cells extracted from organic soils
journal, December 2011
- Dörsch, Peter; Braker, Gesche; Bakken, Lars Reier
- FEMS Microbiology Ecology, Vol. 79, Issue 2
Where old meets new: An ecosystem study of methanogenesis in a reflooded agricultural peatland
journal, December 2019
- McNicol, Gavin; Knox, Sara H.; Guilderson, Thomas P.
- Global Change Biology, Vol. 26, Issue 2
Denitrification gene pools, transcription and kinetics of NO, N2O and N2 production as affected by soil pH: Gene transcription, gas kinetics as affected by soil pH
journal, February 2010
- Liu, Binbin; Mørkved, Pål Tore; Frostegård, Åsa
- FEMS Microbiology Ecology, Vol. 72, Issue 3
The effect of land cover type and structure on evapotranspiration from agricultural and wetland sites in the Sacramento–San Joaquin River Delta, California
journal, June 2018
- Eichelmann, Elke; Hemes, Kyle S.; Knox, Sara H.
- Agricultural and Forest Meteorology, Vol. 256-257
A comparison of two 16S rRNA gene-based PCR primer sets in unraveling anammox bacteria from different environmental samples
journal, November 2013
- Han, Ping; Huang, Yu-Tzu; Lin, Jih-Gaw
- Applied Microbiology and Biotechnology, Vol. 97, Issue 24
Ammonia-Oxidizing Archaea and Bacteria Differentially Contribute to Ammonia Oxidation in Sediments from Adjacent Waters of Rushan Bay, China
journal, February 2018
- He, Hui; Zhen, Yu; Mi, Tiezhu
- Frontiers in Microbiology, Vol. 9
Emissions of N 2 O from Alfalfa and Soybean Crops in Eastern Canada
journal, March 2004
- Rochette, Philippe; Angers, Denis A.; Bélanger, Gilles
- Soil Science Society of America Journal, Vol. 68, Issue 2
Oxygen-limited autotrophic nitrification–denitrification (OLAND) in a rotating biological contactor treating high-salinity wastewater
journal, November 2005
- Windey, Kim; De Bo, Inge; Verstraete, Willy
- Water Research, Vol. 39, Issue 18
amoA-encoding archaea in wastewater treatment plants: a review
journal, January 2013
- Limpiyakorn, Tawan; Fürhacker, Maria; Haberl, Raimund
- Applied Microbiology and Biotechnology, Vol. 97, Issue 4
Effects of seasonality, transport pathway, and spatial structure on greenhouse gas fluxes in a restored wetland
journal, January 2017
- McNicol, Gavin; Sturtevant, Cove S.; Knox, Sara H.
- Global Change Biology, Vol. 23, Issue 7
The microbial nitrogen-cycling network
journal, February 2018
- Kuypers, Marcel M. M.; Marchant, Hannah K.; Kartal, Boran
- Nature Reviews Microbiology, Vol. 16, Issue 5
Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms
journal, January 2011
- Verhamme, Daniel T.; Prosser, James I.; Nicol, Graeme W.
- The ISME Journal, Vol. 5, Issue 6
Mitigation potential of soil carbon management overestimated by neglecting N2O emissions
journal, February 2018
- Lugato, Emanuele; Leip, Adrian; Jones, Arwyn
- Nature Climate Change, Vol. 8, Issue 3
Diversity and abundance of ammonia-oxidizing archaea and bacteria in polluted mangrove sediment
journal, November 2011
- Cao, Huiluo; Li, Meng; Hong, Yiguo
- Systematic and Applied Microbiology, Vol. 34, Issue 7
Relative abundance of denitrifying and DNRA bacteria and their activity determine nitrogen retention or loss in agricultural soil
journal, August 2018
- Putz, Martina; Schleusner, Philipp; Rütting, Tobias
- Soil Biology and Biochemistry, Vol. 123
Potential for negative emissions of greenhouse gases (CO 2 , CH 4 and N 2 O) through coastal peatland re-establishment: Novel insights from high frequency flux data at meter and kilometer scales
journal, March 2018
- Windham-Myers, Lisamarie; Bergamaschi, Brian; Anderson, Frank
- Environmental Research Letters, Vol. 13, Issue 4
Net soil–atmosphere fluxes mask patterns in gross production and consumption of nitrous oxide and methane in a managed ecosystem
journal, January 2016
- Yang, Wendy H.; Silver, Whendee L.
- Biogeosciences, Vol. 13, Issue 5
The legacy of wetland drainage on the remaining peat in the Sacramento — San Joaquin Delta, California, USA
journal, March 2009
- Drexler, Judith Z.; Fontaine, Christian S.; Deverel, Steven J.
- Wetlands, Vol. 29, Issue 1
A genomic perspective on stoichiometric regulation of soil carbon cycling
journal, July 2017
- Hartman, Wyatt H.; Ye, Rongzhong; Horwath, William R.
- The ISME Journal, Vol. 11, Issue 12
Citrate-Ascorbate as a Highly Selective Extractant for Poorly Crystalline Iron Oxides
journal, January 1997
- Reyes, I.; Torrent, J.
- Soil Science Society of America Journal, Vol. 61, Issue 6