Variations of dissimilatory nitrate reduction processes along reclamation chronosequences in Chongming Island, China

https://doi.org/10.1016/j.still.2020.104815Get rights and content

Highlights

  • Dissimilatory nitrate reduction rates increased along reclamation chronosequences.

  • The rates varied due to the altered soil physicochemical characteristics.

  • Denitrification was the dominant pathway contributing to total nitrate reduction.

  • N2O emission was stimulated significantly along reclamation chronosequences.

  • More reactive nitrogen was exported in converted paddy soil than in coastal wetland.

Abstract

Conversion of coastal wetland to paddy soil can significantly affect soil biogeochemistry cycling. However, the impacts of coastal wetland reclamation on dissimilatory nitrate reduction processes and nitrogen fate remain poorly understood. In this study, the effects of coastal wetland reclamation on the rates and related functional gene abundances of dissimilatory nitrate reduction processes, N2O emission, and the fate of reactive nitrogen were investigated in Chongming Island, China. Conversion of coastal wetland to paddy soil can significantly increase dissimilatory nitrate reduction rates. Denitrification was the dominant pathway contributing to the total nitrate reduction, while anammox and DNRA played an important role. Conversion of coastal wetland to paddy soil can significantly affect soil physicochemical characteristics and abundances of related functional genes, leading to the variations of nitrate reduction rates. Although the nitrate removal rates increased along the reclamation chronosequences, due to the intensive N fertilizer application and increased nitrification and ammonification rates, more reactive N can be exported in paddy soil than in wetland, and N2O emission was stimulated significantly along reclamation chronosequences. This study can provide valuable insights into the mechanisms of reclamation influences on soil N recycling.

Introduction

Over the past few decades, overloaded reactive nitrogen transported into coastal areas has caused various environmental issues, especially aquatic eutrophication (Cui et al., 2013; Hou et al., 2015; Chen et al., 2016). Coastal wetlands are key transitional zones between terrestrial ecosystem and marine ecosystem, which can provide extensive ecosystem services in global biogeochemical cycles such as storm protection (Moeller et al., 2014), carbon storage (Duarte et al., 2005), and habitat for flora and fauna (Roberts et al., 2012). Besides, coastal wetlands can filter contaminants including reactive nitrogen from terrestrial ecosystem to open seas (Canfield et al., 2010), and nitrogen removal in coastal wetland can significantly alleviate N loading to the coastal ocean (Peng et al., 2016). Dissimilatory nitrate reduction processes (DNRP) such as denitrification (DNF), anaerobic ammonium oxidation (anammox) and dissimilatory nitrate reduction to ammonium (DNRA) are major pathways of nitrate reduction in coastal wetland, playing an important role in controlling the nitrate dynamics and fate in estuarine and coastal ecosystems (Deng et al., 2015; Gao et al., 2017).

Nowadays, about 50% of the global coastal wetlands have been reclaimed due to the demand for farming and housing (Barbier et al., 2011), and rice planting is a long-term implement in wetland reclamation with great agronomic significance (Zong et al., 2007). Rice paddy is an important way of agricultural cultivation with high amounts of fertilizer N (up to 250 kg N ha−1) and low efficiency of N use (below 40%) (Cassman, 1999; Peng et al., 2006). The conversion of coastal wetland into paddy soil can alter soil physicochemical properties due to fertilization application and other agricultural management (Cui et al., 2012; Ding et al., 2017), and changes of soil physicochemical properties are important factors affecting nitrogen cycling and N2O emission (Li et al., 2015; Liu et al., 2016). For example, long-term application of N fertilization can significantly increase rates of DNF, mineralization and nitrogen fixation in soils (Wu et al., 2017a; Wang et al., 2019; Peng et al., 2016). Therefore, conversion of coastal wetland into paddy soil may significantly increase N loading to coastal regions and affect global warming. Although DNRP in rice paddy soils has been previously studied (Pandey et al., 2019; Shan et al., 2016, 2018), the effects of reclamation chronosequences in coastal wetland on DNRP are poorly understood.

There was extensive reclamation of coastal wetland to paddy soil in the Yangtze River Delta (Zong et al., 2007). As the largest estuarine island in China, approximately half of the present area of Chongming Island were obtained through coastal wetland reclamation (Cui et al., 2012a). Previous studies indicated an increasing trend of nutrients and bacterial diversity and decreasing trend of amorphous Fe oxyhydrates along reclamation chronosequences in the Chongming Island (Cui et al., 2012a, Cui et al., 2012b). However, the knowledge of soil DNRP and related functional gene abundances succession along the rice cultivation chronosequences are still limited. The objectives of this study were to (1) expound the evolution of DNRP, related functional genes abundances, and N2O emission along reclamation chronosequences; (2) identify the main factors regulating DNRP and N2O emission; (3) reveal the fate and environmental implications of N transformation in coastal wetland reclamation. This study can improve the understanding of N removal and transformation in agricultural land and coastal wetland.

Section snippets

Study area and sampling

Chongming Island locates in the Yangtze Estuary with a total area of 1267 km2, which is the largest estuarine island in China (Ma et al., 2015). The average temperature, precipitation and groundwater table of Chongming Island are 15.3 °C, 1003.7 mm and 85.7 cm, respectively. In the reclaimed areas of Chongming Island, nearly 300 kg ha-1 N fertilizers were applied annually, and 15-30 cm high of stubbles were returned to soil after harvesting in the paddy fields (Cui et al., 2012a). The southern

Physicochemical properties

Significant differences were observed in concentrations of NO2, NH4+, NO3, Fe2+, TOC, and sulfides between paddy soil and coastal wetland sediment (one-way ANOVA, p < 0.05), while similar concentrations of Fe3+ were detected. Concentrations of NO2, sulfides and TOC were higher in paddy soil than coastal wetland sediment, and concentrations of NH4+ and Fe2+ were higher in paddy soil than high tidal flats. Contrarily, concentrations of NO3 were lower in paddy soil than coastal wetland

Discussion

Land use change can shift a set of soil abiotic and biotic properties (Aon and Colaneri, 2001; Liu et al., 2018; Singh et al., 2010), and further significantly alter nitrogen cycling processes (Van Lent et al., 2015). Long-term nitrogen (N) fertilization on agricultural soil have caused significant imbalance in biogeochemical N cycling (Galloway et al., 2004; Pandey et al., 2019), nitrous oxide emissions (Liu et al., 2016) and soil microbial communities (Manoharan et al., 2017).

In this study,

Conclusions

This study reported the effects of coastal wetland conversion to paddy soil on DNRP in eastern intertidal flat of Chongming Island, China. Conversion of coastal wetland to paddy soil can significantly increase the rates of DNF, anammox and DNRA, and the nitrate reduction rates generally increased along the reclamation chronosequences. Coastal wetland conversion to paddy soil regulated soil physicochemical characteristics and abundances of related functional genes, further leading to the

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 funded by National Natural Science Foundations of China (grant numbers 41730646, 41761144062, 91851111, 41725002, 41671463, 41501524 and 41971105), and Chinese National Key Programs for Fundamental Research and Development (grant numbers 2016YFE0133700, and 2016YFA0600904). Data presented in this paper can be obtained by sending a written request to the corresponding author.

References (79)

  • A. Lagomarsino et al.

    Soil organic carbon distribution drives microbial activity and functional diversity in particle and aggregate-size fractions

    Pedobiologia

    (2012)
  • J.G. Li et al.

    Evolution of soil properties following reclamation in coastal areas: A review

    Geoderma

    (2014)
  • P.P. Li et al.

    Soil aggregate size and long-term fertilization effects on the function and community of ammonia oxidizers

    Geoderma.

    (2019)
  • Z.G. Li et al.

    Factors affecting the treatment of reject water by the anammox process

    Bioresource. Technol.

    (2011)
  • D. Liu et al.

    Soil physicochemical and microbial characteristics of contrasting land-use types along soil depth gradients

    Catena

    (2018)
  • W.Z. Liu et al.

    Catchment agriculture and local environment affecting the soil denitrification potential and nitrous oxide production of riparian zones in the Han River Basin, China

    Agr. Ecosyst. Environ.

    (2016)
  • L. Manoharan et al.

    Agricultural land use determines functional genetic diversity of soil microbial communities

    Soil. Biol. Biochem.

    (2017)
  • B. Molinuevo et al.

    Anammox for ammonia removal from pig manure effluents: Effect of organic matter content on process performance

    Bioresource. Technol.

    (2009)
  • Y. Ouyang et al.

    Effect of nitrogen fertilization on the abundance of nitrogen cycling genes in agricultural soils: A meta-analysis of field studies

    Soil. Biol. Biochem.

    (2018)
  • A. Pandey et al.

    Dissimilatory nitrate reduction to ammonium dominates nitrate reduction in long-term low nitrogen fertilized rice paddies

    Soil. Biol. Biochem.

    (2019)
  • S.B. Peng et al.

    Strategies for overcoming low agronomic nitrogen use efficiency in irrigated rice systems in China

    Field. Crop. Res.

    (2006)
  • J. Reyes-Avila et al.

    Simultaneous biological removal of nitrogen, carbon and sulfur by denitrification

    Water. Res.

    (2004)
  • F. Sgouridis et al.

    Denitrification and dissimilatory nitrate reduction to ammonium (DNRA) in a temperate re-connected floodplain

    Water. Res.

    (2011)
  • J. Shan et al.

    Tetracycline and sulfamethazine alter dissimilatory nitrate reduction processes and increase N2O release in rice fields

    Environ. Pollut.

    (2018)
  • R.B. Sun et al.

    Effects of long-term application of chemical and organic fertilizers on the abundance of microbial communities involved in the nitrogen cycle

    Appl. Soil. Ecol.

    (2015)
  • C. Wang et al.

    Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition

    Soil. Biol. Biochem.

    (2018)
  • J. Wang et al.

    A novel sulfate reduction, autotrophic denitrification, nitrification integrated (SANI) process for saline wastewater treatment

    Water. Res.

    (2009)
  • X. Wu et al.

    Effects of land-use change and fertilization on N2O and NO fluxes, the abundance of nitrifying and denitrifying microbial communities in a hilly red soil region of southern China

    Appl. Soil. Ecol.

    (2017)
  • L. Wu et al.

    Conversion from rice to vegetable production increases N2O emission via increased soil organic matter mineralization

    Sci. Total. Environ.

    (2017)
  • B. Yi et al.

    Alteration of gaseous nitrogen losses via anaerobic ammonium oxidation coupled with ferric reduction from paddy soils in Southern China

    Sci. Total. Environ.

    (2019)
  • G.Y. Yin et al.

    Effects of thiamphenicol on nitrate reduction and N2O release in estuarine and coastal sediments

    Environ. Pollut.

    (2016)
  • E.B. Barbier et al.

    The value of estuarine and coastal ecosystem services

    Ecol. Monogr.

    (2011)
  • A.J. Burgin et al.

    Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways

    Front. Ecol. Environ.

    (2007)
  • D.E. Canfield et al.

    The evolution and future of Earth’s nitrogen cycle

    Science

    (2010)
  • K.G. Cassman

    Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture

    Proc. Natl. Acad. Sci.

    (1999)
  • F. Chen et al.

    Net anthropogenic nitrogen inputs (NANI) into the Yangtze River basin and the relationship with riverine nitrogen export

    J. Geophys. Res. Biogeosci.

    (2016)
  • J. Cui et al.

    Bacterial succession during 500 years of soil development under agricultural use

    Ecol. Res.

    (2012)
  • S.H. Cui et al.

    Centennial-scale analysis of the creation and fate of reactive nitrogen in China (1910-2010)

    Proc. Natl. Acad. Sci.

    (2013)
  • E.A. Davidson et al.

    Temperature sensitivity of soil carbon decomposition and feedbacks to climate change

    Nature

    (2006)
  • Cited by (10)

    • Antibiotics sulfamethoxazole alter nitrous oxide production and pathways in estuarine sediments: Evidenced by the N<sup>15</sup>-O<sup>18</sup> isotopes tracing

      2022, Journal of Hazardous Materials
      Citation Excerpt :

      Additionally, total N2O production rates were found to be positively associated with NO2- concentration, PNIT rates, URE activity, 16 S rRNA, AOB, hao, nirK gene abundances and nirK: nosZ ratio, while negatively associated with NO3-, nirS gene abundance and nirS: nosZ ratio (p < 0.05) (Fig. S4). Ambient N2O production rates in this work (0.41 nmol g−1 h−1) were consistent with previous studies in intertidal wetlands of the Yangtze Estuary (Gao et al., 2019; Jiang et al., 2021). Dual-isotope (15N–18O) labeling experiments results demonstrated that ND dominated N2O production in this region, which accounted for 39.5–76.4% of total N2O production, followed by NCD (0–44.9%), HD (23.6%) and NN (0–9.2%).

    • The relative dominance of denitrification and dissimilatory nitrate reduction to ammonium (DNRA) under four vegetation types in a typical coastal wetland

      2022, Applied Soil Ecology
      Citation Excerpt :

      NO3− is usually used by bacteria as electronic acceptors during NO3− reduction (Irving et al., 2011; Shu et al., 2021). Soil organic carbon (SOC) and NO3− loading rates are two key factors in determining DNF and DNRA (Her and Huang, 1995; Jiang et al., 2021). Meanwhile, suitable soil pH (neutral or slightly alkaline conditions) could increase soil bacterial abundance diversity and corresponding nutrient cycling activities, and affect DNF and DNRA (Rousk et al., 2009; Shi et al., 2020).

    • Metagenomics highlights the impact of climate and human activities on antibiotic resistance genes in China's estuaries

      2022, Environmental Pollution
      Citation Excerpt :

      Total organic carbon (TOC) was analyzed using a CHNOS Elementary Analyzer (Vario EL III) after extracting with 2 mol L−1 HCl (Hou et al., 2018). Sulfide (S) was analyzed by an Orion Sure-flow Combination silver-sulfide electrode (Thermo Scientific Orion) (Jiang et al., 2021). Fe2+ and Fe3+ were detected using a Photometric Ferrozine Assay after extracting by 0.5 g sediment with 30 mL of 0.5 mol L−1 HCl from sediment (Yin et al., 2015).

    • Sulfur transformation and bacterial community dynamics in both desulfurization-denitrification biofilm and suspended activated sludge

      2022, Bioresource Technology
      Citation Excerpt :

      The functional genes related to the nitrogen transformation included the dissimilatory nitrate reduction genes, the assimilatory nitrate reduction genes, and the denitrification genes, as shown in Fig. 5. The dissimilatory nitrate reduction (NO2– to NH3) was realized via the nitrate reductase encoded by nirB, nirD, nrfH and nrfA (Jiang et al., 2021). The abundance of dissimilatory nitrate reduction genes in biofilms was higher than in the suspended sludge, indicating some NO2– around the biofilm was converted to NH3 rather than N2.

    View all citing articles on Scopus
    View full text