Long term combined fertilization and soil aggregate size on the denitrification and community of denitrifiers
Introduction
Fertilization processes are indispensable management tools for enhancing soil nutrition and crop yields in a majority of agricultural ecosystems, and are known to influence the microbial regulated nitrogen (N) cycling processes (Hallin et al., 2009). However, the intensive use of fertilizers increase soil denitrification, and nitrate is reduced to nitrogen gas, which potentially generates greenhouse gases, such as nitrous oxide (N2O) (Syakila and Kroeze, 2011; Akiyama et al., 2013). Approximately 60% of the global N2O emissions originate from agricultural soils (IPCC, 2014).
N2O is an atmospheric trace gas with relatively long lifetime. Increase in concentration of N2O contributes to global warming and damages the ozone layer. In recent years, the excessive use of mineral nitrogen (N) fertilizers has increased N2O threat (Frink et al., 1999; Liu et al., 2013). Therefore, practices with reduced fertilizers and energy inputs have recommended globally (Mäder et al., 2002). The Chinese government has recommended inorganic fertilizer reduction management practices for environment protection particularly in North China Plain, which is a major grain producing region with intensive double-crop wheat/maize rotation where the use and application of chemical N is high (Guo et al., 2010).
Several studies have demonstrated that reduced quantity of inorganic N fertilizers efficiently reduced denitrification and N2O emission (Ding et al., 2007; Wang et al., 2009). However, long-term reduced inorganic N may reduce soil fertility and grain production in North China Plain, where calcareous fluvo-aquic soil is predominant. Application of organic manure in combination with reduced quantity of chemical fertilizers is considered effective to maintain crop yield (Zhao et al., 2016; Zhang et al., 2016). When reduced inorganic N combined organic fertilizers, an increase in N2O emissions was detected. Efforts have been made to reveal the mechanism and their regulatory microorganisms (Jäger et al., 2011; Cui et al., 2016). However, knowledge on microbial denitrification under long-term combined use of organic and reduced inorganic fertilizers is far from complete and is yet to account for biological variation among soil types and the diverse range of farming systems.
Nitrite (NO2−) reduction to nitric oxide (NO) is a key step in denitrification. This conversion is catalyzed by nitrite reductases of denitrifying bacteria. Nitrite reductases are of two types: copper-containing reductase (nirK) and cytochrome cd1-containing reductase (nirS) (Zumft, 1997). Historically, nirK and nirS genes have been widely utilized as molecular markers to investigate the denitrifiers of different terrestrial ecosystems (Hallin and Lindgren, 1999; Chen et al., 2010; Wei et al., 2015) and under different fertilizer sources or types (Brenzinger et al., 2018; Dai et al., 2019). Some researchers have demonstrated that nirS denitrifiers were susceptible to organic fertilizers particularly in upland soils (Tang et al., 2010; Yin et al., 2015; Cui et al., 2016). In contrast, Chen et al. (2010) reported that nirK denitrifiers were responsive to organic fertilization in a paddy soil. Furthermore, nirK gene outnumbered nirS gene in paddy ecosystems (Yoshida et al., 2010; Yuan et al., 2012; Azziz et al., 2017).
Abundance and community structure of denitrifiers depend on soil type (Cavigelli and Robertson, 2000). Studies on nirK- and nirS-denitrifying bacteria under a broad range of soils have implied that the two denitrifiers occupy different ecological niches (Priemé et al., 2002; Braker et al., 2015). Soil fertility management may change the soil environment, which influences the structural and functional differentiation of the microbial community. The two types of denitrifiers and their contribution to potential denitrification may vary depending on long-term combined use of organic and inorganic fertilizers.
Fertilizer management practices can affect soil aggregate distribution. Aggregates are important soil components that provide spatially heterogeneous microclimatic conditions, including water, air, and nutrition, for soil microbes (Mäder et al., 2002; Bach and Hofmockel, 2014). Soil aggregate distribution is directly influenced by fertilization, while soil aggregate size can modify the impacts of fertilization on microbial communities (F.Q. Li et al., 2019). Studies have proven differences in N2O production in heterogeneous soil aggregate size classes under different fertilization conditions (Uchida et al., 2008; Diba et al., 2011). However, the response of these denitrifying populations to changes in different aggregates size at the microlevel has rarely been investigated.
Here, we investigate the effects of long-term straw or manure application paired with reduced quantity of chemical fertilizer and soil aggregates of different size classes on denitrification and N2O emission in calcareous fluvo-aquic soil. The abundance and community structures of the denitrifiers within soil aggregates under different fertilizer management practices were analyzed for the following reasons: (1) to understand the effects of straw and manure application on denitrifiers in the aggregates and the possible mechanisms via which denitrification is enhanced or inhibited; (2) to identify the soil physicochemical factors that determine the distribution of nirK and nirS-type denitrifiers in soil aggregates and their correlation with denitrification under different fertilizer management practices; and (3) to compare the aggregate size effects on the abundance, diversity, and community composition of the nirK and nirS-type denitrifiers.
Section snippets
Study site
The experiment site near Yellow River located in Yuanyang County of Henan Province (35°00′ 28″ N, 113° 41′48″E) had a rotational cropping system involving winter wheat and summer maize. The soil of this site was classified as Calcaric cambisol (IUSS Working Group WRB, 2007). This region had a temperate monsoon climate with an annual average temperature of 14.7 °C and precipitation of 645 mm. Four types of fertilizer applications, including control without fertilizers (Control); fertilization
Soil properties and potential denitrification activities
Our previous study demonstrates the effects of fertilization and aggregate size on soil pH, moisture, SOC, NH4+-N, and NO3−-N, and TN (P.P. Li et al., 2019). NPKS and NPKM treatments resulted in lower soil pH higher moisture, SOC, and TN; soil aggregate size significantly affected NH4+-N and SOC with higher values of the microaggregates.
The present study analyzed PDA in bulk soils and in soil aggregates under control and fertilization treatments (Fig. 1). The PDA in bulk soils ranged from
Effects of fertilization practice and soil aggregate size on denitrification potential
Consistent with our hypothesis, PDA was more in the straw- and manure-amended treatments (NPKS and NPKM) than in the control and NPK treatments. The significantly higher PDA in small macroaggregates and microaggregates indicated that these smaller soil aggregates may be the denitrification hot spots, which potentially generated more N2O, particularly in the NPKS and NPKM treatments. Uchida et al. (2008) previously demonstrated increased N2O emission from smaller soil aggregates following cow
Conclusions
In this study, microbe-mediated denitrification under long-term combined organic and inorganic fertilization at the soil aggregate level was analyzed. The combined application of organic and inorganic nitrogen (N) fertilization significantly stimulated soil denitrification activities. A dramatic increase with combined fertilization was observed in the small macroaggregates and microaggregates with greater increase in nirS gene abundance. Functional gene (nirS and nirK) abundance and
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 financially supported by the Natural Science Foundation of China (41401273), National Key Research and Development Program of China (2017YFD0301103).
References (64)
- et al.
nirS- and nirK-type denitrifier communities are differentially affected by soil type, rice cultivar and water management
Eur. J. Soil Biol.
(2017) - et al.
Soil aggregate isolation method affects measures of intra-aggregate extracellular potential
Soil Biol. Biochem.
(2014) - et al.
Morphology, lacunarity and entropy of intra aggregate pores: aggregate size and soil management effects
Geoderma
(2008) - et al.
Annual emissions of nitrous oxide and nitric oxide from a wheat–maize cropping system on a silt loam calcareous soil in the North China plain
Soil Biol. Biochem.
(2012) - et al.
Long-term organic and inorganic fertilization alters temperature sensitivity of potential N2O emissions and associated microbes
Soil Biol. Biochem.
(2016) Advances in characterization of soil structure
Soil Till. Res.
(1988)- et al.
Nitrous oxide emissions from an intensively cultivated maize–wheat rotation soil in the North China plain
Sci. Total Environ.
(2007) - et al.
Influence of crop rotation and aggregate size on carbon dioxide production and denitrification
Soil Till. Res.
(2004) - et al.
Correlations between in situ denitrification activity and nir-gene abundances in pristine and impacted prairie streams
Environ. Pollut.
(2010) - et al.
Structure and assembly cues for rhizospheric nirK- and nirS-type denitrifier communities in long-term fertilized soils
Soil Biol. Biochem.
(2018)
N2O emission immediately after rainfall in a dry stubble field
Soil Biol. Biochem.
Processes and factors controlling N2O production in an intensively managed low carbon calcareous soil under sub-humid monsoon conditions
Environ. Pollut.
Soil aggregate size modifies the impacts of fertilization on microbial communities
Geoderma
Soil aggregate size and long-term fertilization effects on the function and community of ammonia oxidizers
Geoderma
Effects of soil chemical characteristics and water regime on denitrification genes (nirS, nirK, and nosZ) abundances in a created riverine wetland complex
Ecol. Eng.
The effect of soil aggregate size on pore structure and its consequence on emission of greenhouse gases
Soil Till. Res.
Nitrogen oxide emissions from an irrigated maize crop amended with treated pig slurries and composts in a Mediterranean climate
Agr. Ecos. Environ.
Crop residue influence on denitrification, N2O emissions and denitrifier community abundance in soil
Soil Biol. Biochem.
Potential for denitrification in cereal soils of northern Australia after legume or grass-legume pastures
Soil Biol. Biochem.
N2O emission and the N2O/(N2O + N2) product ratio of denitrification as controlled by available carbon substrates and nitrate concentrations
Agri. Ecos. Environ.
Effects of combined biochar and organic fertilizer on nitrous oxide fluxes and the related nitrifier and denitrifier communities in a saline-alkali soil
Sci. Total Environ.
Phases of denitrification following oxygen depletion in soil
Soil Biol. Biochem.
Nitrous oxide emission and denitrifier communities in drip-irrigated calcareous soil as affected by chemical and organic fertilizers
Sci. The Total Environ.
Effects of aggregate size, soil compaction, and bovine urine on N2O emissions from a pasture soil
Soil Biol. Biochem.
Modelling and predicting crop yield, soil carbon and nitrogen stocks under climate change scenarios with fertiliser management in the North China Plain
Geoderma
Effects of organic–inorganic compound fertilizer with reduced chemical fertilizer application on crop yields, soil biological activity and bacterial community structure in a rice–wheat cropping system
Appl. Soil Ecol.
Nitrification, ammonia-oxidizing communities, and N2O and CH4 fluxes in an imperfectly drained agricultural field fertilized with coated urea with and without dicyandiamide
Biol. Fertil. Soils
Impact of land use management and soil properties on denitrifier communities of Namibian Savannas
Microbiol. Ecol.
pH-driven shifts in overall and transcriptionally active denitrifiers control gaseous product stoichiometry in growth experiments with extracted bacteria from soil
Front. Microbiol.
Organic residue amendments to modulate greenhouse gas emissions from agricultural soils
Front. Microbiol.
The functional significance of denitrifier community composition in a terrestrial ecosystem
Ecology
Impact of long-term fertilization on the composition of denitrifier communities based on nitrite reductase analyses in a paddy soil
Microb. Ecol.
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Pei-Pei Li & Shui-Qing Zhang contributed equally to this work.