Restoring wetlands on intensive agricultural lands modifies nitrogen cycling microbial communities and reduces N2O production potential

https://doi.org/10.1016/j.jenvman.2021.113562Get rights and content

Highlights

  • Land use type is the main determinant for N2O production potential in the Delta.

  • All processes (nitrification, denitrification, DNRA) contribute to N2O production.

  • Drained soils show the highest N2O production potential.

  • Wetland restoration will increase the potential for N2O reduction to N2.

  • Restored wetlands in the Delta have high nitrogen fixing 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, 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.

Introduction

Nitrous oxide (N2O) is a GHG with a 298-fold greater warming potential than carbon dioxide (CO2) and is involved in the destruction of stratospheric ozone layer. High N2O emissions mainly originate in soil ecosystems, particularly in drained agricultural soils. Pressure to the agricultural sector is increasing as the global population and the demand for food grows. In recent years, the excessive use of nitrogen-based fertilizers has greatly contributed to the elevated N2O concentrations (Park et al., 2012), and it has been predicted that farmlands and fertilizer applications will increase 35–60% before 2030, and therefore it is expected that these agricultural soils will contribute up to 59% of total N2O emission (US EPA, 2012).

Since the agricultural sector plays a crucial role in N2O emissions (Tian et al., 2020), it is essential to understand how the underlying mechanisms in soil lead to N2O productions and emission, as well as to potential consumption by soil microorganisms. Soil nutrient ratios and availability, soil moisture, vegetation species and density, and temperature are the most important factors for microbes performing nitrogen (N) transforming processes (Firestone et al., 1980; Liimatainen et al., 2018; Pärn et al., 2018). Therefore, it is crucial to understand how N transforming potential will vary among intensively managed arable lands and how these emissions change if these managed soils undergo land-use change, such as restoration to wetlands. Restored and natural wetlands have already proven to be effective to sequester carbon (C) from the atmosphere (Hemes et al., 2019), and since the N2O emission from natural wetlands is considered negligible, this suggests that wetland restoration could lead to significantly lower N2O production potential.

The Sacramento-San Joaquin Delta (hereafter referred to as the Delta) is California's most important agricultural area, which is highly vulnerable to inundation due to the subsided agricultural peat soils. Some of the areas in the Delta are now up to 9 m below sea level, and more than 1500 km of levees and dams are protecting the area from flooding (Drexler et al., 2009). To reverse the soil subsidence, wetland restoration activities have been underway for more than two decades, and many studies have shown restoration to be a highly efficient measure to build up lost soils (Chamberlain et al., 2018; Eichelmann et al., 2018; Hemes et al., 2019). However, most of the focus has been on reducing CO2 emissions for intensively managed agricultural sites and better quantifying the effects of methane (CH4) emissions on the wetland ecosystem greenhouse gas balance after re-wetting (Hemes et al., 2018a, McNicol et al., 2020).

Short-term weekly ebullition chamber and dissolved N2O measurements at a restored and a natural nearby wetland at the Delta showed insignificant N2O emissions that had negligible effect on the ecosystem GHG budget (McNicol et al., 2017; Pärn et al., 2018), while corn, alfalfa and pasture have shown to be moderate to large N2O sources. For example, Hemes et al. (2019) showed that the N2O emissions detected with automated chambers from corn and alfalfa were 3.28 ± 0.12 g N2O–N m−2 yr−1 and 0.51 ± 0.07 g N2O–N m−2 yr−1, respectively. Measurements at pasture sites by (Teh et al., 2011) and (Pärn et al., 2018) have shown a similar range, where the emission was 2.4 ± 1.3 g N2O–N m−2 yr−1 and 0.61 ± 0.27 g N2O–N m−2 yr−1, respectively. First long term N2O measurements over the Delta agricultural peatlands showed very high emissions where the total N2O fluxes averaged 26 ± 0.5 kg N2O-N ha-1 yr-1 (Anthony and Silver, 2021). These studies have clearly shown that N2O emissions from different land use types at the Delta will vary substantially, being lower in wetland ecosystems and larger in agricultural systems.

Extensive research to understand the stoichiometric regulation of soil C cycling at a Delta rice fields has been carried out by Hartman et al. (2017). However, no analyses in terms of N cycling processes are available. The N cycle is driven by abiotic and biotic (i.e., decomposition, mineralization, assimilative and dissimilative) processes (Espenberg et al., 2018), which include different microbial pathways, such as N fixation, nitrification, denitrification, dissimilatory nitrate reduction to ammonium (DNRA) and anaerobic ammonium oxidation (ANAMMOX) (Kuypers et al., 2018). The abundance of functional genes of microbes involved in N cycling has been shown in many studies to be effective in predicting the potential of N cycling processes (Jones et al., 2014) in various ecosystems, including agricultural soils (Long et al., 2013) and natural and restored wetlands (Han et al., 2013; Ligi et al., 2015). In denitrification, the abundance of nirK and nirS genes refers to the N2O emission potential, and the abundance of nosZI and nosZII genes indicates the potential for N2O reduction, which is the only known biological sink for N2O (Spiro, 2012). The other organisms which may change the N balance between soil and atmosphere are ammonium oxidizing bacteria (AOB) and archaea (AOA), ANAMMOX-specific bacteria, N-fixers, and microbes carrying out DNRA.

The main aim of this study is to understand how the abundance of N cycling functional genes has changed after the restoration of wetlands from intensively managed agricultural sites in the Delta. Based on the previous knowledge, we hypothesized that: (i) organic-rich drained soils have higher potential for N2O production and emissions; (ii) wetland restoration would increase the abundance of N2O reducers and decrease the abundance of ammonia oxidizers, leading to less N2O emission in restored wetlands due to the anaerobic conditions; and (iii) lower soil temperature at the wetlands reduce the potential for N2O production. If true, these hypothesized drivers and land-use patterns of N2O emissions reductions could provide further incentive for agriculture to wetland restoration.

Section snippets

Site description

The seven sites analyzed in this study are located on Twitchell, Sherman and Bouldin Islands and are composed of four restored wetlands and three agricultural sites. The mean annual air and soil temperature measured close to the flux tower from topsoil layer (<15 cm depth) is shown in Table 1. All sites experience similar mean annual precipitation of 338 mm. Although being in a proximity with similar annual air temperature and precipitation, the sites experience a wide variety of management

Soil properties

The various land management practices in the Delta resulted in significant differences in soil properties. The difference was observable among wetland sites but also between wetlands and agricultural sites. Soil C% and N% was highest in West Pond, Mayberry, and corn where the mean values were for C were 17.0 ± 2.6%, 15.6 ± 3.6%, and 15.4 ± 1.1% and 1.09 ± 0.1%, 1.0 ± 0.25%, and 1.12 ± 0.08% for N, respectively. East End, Sherman Wetland, alfalfa, and pasture had significantly lower values

Discussion

Nitrous oxide is the third most important well-mixed greenhouse gas, and its concentration in the atmosphere is strongly related to land management. Here we analyzed how the abundance of N-cycling genes changes from intensively managed agricultural sites to restored wetlands of different ages in the Delta. Due to the extensive drainage, water table fluctuations, and fertilizer use, many agricultural sites in the Delta have been revealed to be significant N2O sources (Deverel et al., 2017; Hemes

Conclusions

Drained and fertilized agricultural sites are globally important N2O sources, and their contribution to emissions of this ozone-depleting greenhouse gas is increasing annually as more land is converted for agricultural use. Our research has shown that the highest N2O production potential in the studied Delta ecosystems is from the intensively managed organic-rich agricultural sites. The abundance of nirS and nirK genes at the organic-rich corn site significantly exceeded the abundance at all

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This work was supported by the California Department of Water Resources through a contract from the California Department of Fish and Wildlife and the United States Department of Agriculture (NIFA grant #2011-67003-30371). Funding for the AmeriFlux core sites was provided by the U.S. Department of Energy's Office of Science (AmeriFlux contract #7079856). This research was supported by the Estonian Research Council (grants no PSG631, PRG352 and MOBERC20) and by the European Union (EU) through

References (81)

  • M. Putz et al.

    Relative abundance of denitrifying and DNRA bacteria and their activity determine nitrogen retention or loss in agricultural soil

    Soil Biol. Biochem.

    (2018)
  • K. Regan et al.

    Spatial and temporal dynamics of nitrogen fixing, nitrifying and denitrifying microbes in an unfertilized grassland soil

    Soil Biol. Biochem.

    (2017)
  • O.A.L.O. Saad et al.

    Adaptation to temperature of nitric oxide-producing nitrate-reducing bacterial populations in soil

    Syst. Appl. Microbiol.

    (1993)
  • K. Windey et al.

    Oxygen-limited autotrophic nitrification-denitrification (OLAND) in a rotating biological contactor treating high-salinity wastewater

    Water Res.

    (2005)
  • Tyler L. Anthony et al.

    Hot moments drive extreme nitrous oxide and methane emissions from agricultural peatlands

    Glob. Chang. Biol.

    (2021)
  • E.M. Baggs et al.

    Changing pH shifts the microbial source as well as the magnitude of N2O emission from soil

    Biol.Fert.Soil.

    (2010)
  • N.S. Bolan et al.

    Processes of soil acidification during nitrogen cycling with emphasis on legume based pastures

    Plant Soil

    (1991)
  • G. Braker et al.

    Influence of temperature on the composition and activity of denitrifying soil communities

    FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Ecol.

    (2010)
  • F. Carrapiço

    Azolla as a superorganism. Its implication in symbiotic studies

    Cell. Orgin Life Habit. Astrobiol.

    (2010)
  • S.D. Chamberlain et al.

    Soil properties and sediment accretion modulate methane fluxes from restored wetlands

    Global Change Biol.

    (2018)
  • S. Deverel et al.

    Implications for greenhouse gas emission reductions and economics of a changing agricultural mosaic in the sacramento–san Joaquin Delta

    San Franc. Estuary Watershed Sci.

    (2017)
  • P. Dörsch et al.

    Community-specific pH response of denitrification: experiments with cells extracted from organic soils

    FEMS Microbiol. Ecol.

    (2012)
  • S. Dray et al.

    The ade4 package: implementing the duality diagram for ecologists

    J. Stat. Software

    (2007)
  • J.Z. Drexler et al.

    The legacy of wetland drainage on the remaining peat in the Sacramento — san Joaquin Delta, California, USA

    Wetlands

    (2009)
  • M. Ekman et al.

    Proteomic analysis of the cyanobacterium of the Azolla symbiosis: identity, adaptation, and NifH modification

    J. Exp. Bot.

    (2008)
  • M. Espenberg et al.

    Differences in microbial community structure and nitrogen cycling in natural and drained tropical peatland soils

    Sci. Rep.

    (2018)
  • M.K. Firestone et al.

    Nitrous oxide from soil denitrification: factors controlling its biological production

    Science

    (1980)
  • P. Han et al.

    A comparison of two 16S rRNA gene-based PCR primer sets in unraveling anammox bacteria from different environmental samples

    Appl. Microbiol. Biotechnol.

    (2013)
  • W.H. Hartman et al.

    A genomic perspective on stoichiometric regulation of soil carbon cycling

    ISME J.

    (2017)
  • H. He et al.

    Ammonia-oxidizing archaea and bacteria differentially contribute to ammonia oxidation in sediments from adjacent waters of rushan bay, China

    Front. Microbiol.

    (2018)
  • K.S. Hemes et al.

    A biogeochemical compromise: the high methane cost of sequestering carbon in restored wetlands

    Geophys. Res. Lett.

    (2018)
  • K.S. Hemes et al.

    A unique combination of aerodynamic and surface properties contribute to surface cooling in restored wetlands of the sacramento-san Joaquin Delta, California

    J. Geophys. Res.: Biogeosciences

    (2018)
  • S. Humbert et al.

    Abundance of anammox bacteria in different wetland soils

    Environ. Microbiol. Rep.

    (2012)
  • C.M. Jones et al.

    The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink

    ISME J.

    (2013)
  • C.M. Jones et al.

    Recently identified microbial guild mediates soil N 2 O sink capacity

    Nat. Clim. Change

    (2014)
  • P. Kayee et al.

    Archaeal amoA genes outnumber bacterial amoA genes in municipal wastewater treatment plants in Bangkok

    Microb. Ecol.

    (2011)
  • M. Kesik et al.

    Effect of pH, temperature and substrate on N2O, NO and CO2 production by Alcaligenes faecalis p

    J. Appl. Microbiol.

    (2006)
  • L. Klemedtsson et al.

    Soil CN ratio as a scalar parameter to predict nitrous oxide emissions

    Global Change Biol.

    (2005)
  • R. Knowles

    Denitrification

    Microbiol. Rev.

    (1982)
  • M.M.M. Kuypers et al.

    The microbial nitrogen-cycling network

    Nat. Rev. Microbiol.

    (2018)
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