Warmer and drier conditions alter the nitrifier and denitrifier communities and reduce N2O emissions in fertilized vegetable soils

doi:10.1016/j.agee.2016.06.026

Agriculture, Ecosystems & Environment

Volume 231, 1 September 2016, Pages 133-142

https://doi.org/10.1016/j.agee.2016.06.026 Get rights and content

Highlights

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A field study of the impact of simulated climate change on microbial communities and N₂O emissions.
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Warmer and drier conditions led to reduced N₂O emissions.
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Simulated climate change had a more significant impact on ammonia oxidizing bacteria than archaea.
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Simulated climate change increased nirK and decreased nosZ gene abundance.
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N₂O was related to AOB, nirK and nosZ gene abundance.

Abstract

Nitrous oxide (N₂O) is a potent greenhouse gas and is mainly produced from agricultural soils especially vegetable soils with large N fertilizer input. How future projected climate change may impact on the N₂O emissions and the related key (de)nitrifier communities in such ecosystem is poorly understood. The aim of this field study was to determine the interactive effects of a simulated warmer and drier climate on (de)nitrifier communities and N₂O emissions in a vegetable soil. A warmer (+3.3 °C) and drier climate (−14.4% soil moisture content) was created with greenhouses with or without urea N fertilizer application. The variation of microbial population abundance and community structure of Ammonia-oxidizing archaea (AOA), bacteria (AOB) and denitrifiers (nirK/S, nosZ) were determined using Real time-PCR and sequencing. The results showed a strong interactive effect of simulated climate change with N fertilizer applications, whereby the impacts of warmer and drier conditions on the microbial communities and N₂O emissions were more evident when N fertilizer was applied. The simulated warmer and drier conditions in the greenhouses significantly decreased N₂O emissions largely due to the drier soil conditions. The abundance and community structure of AOB showed more rapid responses than AOA under the simulated climate conditions when N fertilizer was applied. Changes of AOB community structure were significantly correlated with soil moisture content and NH₄⁺-N concentration. The simulated climate change did not affect the nirS gene abundance, but significantly increased nirK gene abundance, and significantly decreased nosZ gene abundance with urea application. N₂O emissions were positively correlated with the bacterial amoA abundance and with the ratio of nirK/nosZ gene abundance. Therefore, bacterial amoA, nirK- and nosZ-type denitrifiers are the dominant microbial communities which were affected by the simulated climate conditions and are thus critically important for N cycling in vegetable soils under a changing climate.

Introduction

Nitrous oxide (N₂O) is the third most important greenhouse gas, after carbon dioxide (CO₂) and methane (CH₄), with a global warming potential of about 298 times that of carbon dioxide (CO₂) (IPCC, 2007). It is also the most significant ozone-depleting substance (Ravishankara et al., 2009). Two-thirds of anthropogenic N₂O emissions originate from agriculture soils, especially following the application of nitrogen (N) fertilizers or animal manures (Mosier et al., 1998). To meet the rising global food demands, the amount of N fertilizers used for agricultural production is expected to increase even further (Galloway et al., 2008), potentially leading to rising N₂O emissions. The rising concentrations of greenhouse gases, such as CO₂, CH₄ and N₂O, have already resulted in regional and global climatic changes. It is projected that global surface temperature may rise between 2 and 4 °C by the end of the 21st century and extreme weather patterns such as heat waves accompanied by severe droughts are likely to become more common (IPCC, 2007, IPCC, 2014). These new weather conditions are likely to create new challenges for agricultural production, including nutrient and fertilizer management to feed the growing world population.

Many studies have sought to elaborate on the effect of climate change drivers such as elevated CO₂ (eCO₂), warming and drought on N₂O emissions. On the one hand, these studies were conducted on grassland, heathland, dryland, steppe, and alpine meadow ecosystems (Hu et al., 2010, Hu et al., 2015, Hu et al., 2016, Brown et al., 2012, Cantarel et al., 2011, Cantarel et al., 2012, Carter et al., 2011, Larsen et al., 2011, Hartmann et al., 2013), and revealed that the N₂O fluxes in response to simulated climate change varied with local climate conditions, land use types and agricultural management. Among these factors, agricultural management, such as grazing perturbations and fertilizer application might alter the extent of climatic change effect on N₂O fluxes (Hu et al., 2010, Hartmann and Niklaus, 2012, Hartmann et al., 2013, Tian et al., 2015). These studies suggested that positive effects of warming on N₂O emissions were because warming induced N mineralization, thus increasing N availability in the ecosystem (Cantarel et al., 2011, Cantarel et al., 2012). However, few studies have been reported on the effect of climate change on N₂O emissions from intensive agroecosystems, such as vegetable soils, where large N inputs occur annually (He et al., 2009).

On the other hand, the interactive effects of climate drivers on N₂O emissions were much more complex than single-factor effects. Results from multiple climate change studies indicated that the interactive effects tend to cause smaller changes in N₂O efflux than from single-factor manipulations as the effect of individual treatments may negate each other if they act in opposite directions (e.g. summer drought and warming) (Larsen et al., 2011, Brown et al., 2012). Therefore, single-factor studies might overestimate the effect of climate change on N₂O emissions. Previous studies demonstrated that changed temperature and soil moisture content were two main direct climatic factors that affect N₂O emissions, while the effect of eCO₂ was often indirect through changing soil moisture content and/or nitrogen turnover (Billings et al., 2002, Cantarel et al., 2011, Cantarel et al., 2012, Larsen et al., 2011, Liu et al., 2015). Thus, a study on the interactive effect of warming and drought might be a more effective and realistic approach to understanding the impact of climate change on N₂O emissions in vegetable soils.

Feedback responses of the microorganisms related to N₂O emissions caused by warming and drought were different between different ecosystems and regions (Singh et al., 2010), and their inherent habitus resulted in different sensitivity to changed climate conditions. Nitrifiers (AOA and AOB) are the key drivers of nitrification, which are of vital importance in vegetable soils as it can affect the form of nitrogen that can be used for vegetable growth and nitrogen losses (e.g. NO₃⁻-N leaching and N₂O emission). It was reported that both AOA and AOB were potentially influenced by changed temperature and soil moisture content, although their responses were highly variable in different studies due to different soil parameters (Avrahami and Bohannan, 2009, Gleeson et al., 2010, Chen et al., 2013). Denitrification is a multistep process with each step being mediated by different groups of microorganisms encoded by different functional genes. This process plays an important part in N losses, including N₂O emissions in vegetable soils (Xiong et al., 2006, He et al., 2009, Pang et al., 2009). As denitrifying gene abundances could act as indicators of nitrous oxide emissions from soils (Morales et al., 2010), detailed understanding on denitrifier abundances in response to simulated climate change should be helpful for developing future-proof N₂O mitigation options.

Vegetable soils occupy about 11% of cropland in China, and account for about 20% of the national cropland N₂O emissions (He et al., 2009), far more than that from grassland or forest ecosystems (Brown et al., 2012). However, knowledge on how the projected climate change may impact on N₂O emissions and (de)nitrifiers in vegetable soils, and the feedbacks of these microorganisms through community structural adaption remained scarce. Therefore, corresponding studies on vegetable soils under the projected climate change scenario are needed to bridge this knowledge gap.

We thus conducted an experiment focusing on the interactive effect of warming and drought along with N fertilization on (de)nitrifier communities and N₂O emissions in a vegetable soil. The objectives of this study were to determine possible impacts of simulated climate change (warmer temperatures and drought) in combination with N fertilizer (urea) use on (1) ammonia oxidizing and denitrifying communities; (2) N₂O emissions; and (3) relationships between N₂O emissions and the microbial communities and soil conditions. We hypothesized that the simulated conditions of climate change together with N fertilizer use would alter the ammonia oxidizing and denitrifier communities which in turn would affect N₂O emissions. Greenhouses were built to enable the simulation of warmer (+3.3 °C) and summer drought (−14.4%) to test this hypothesis.

Section snippets

Site description

A field experiment was carried out in an Experimental Station located in Zhejiang University (30°18′N, 120°05′E), Hangzhou, China. This area has a subtropical monsoon climate with an annual average temperature of 17.8 °C and annual rainfall of 1454 mm. Before the establishment of experiment, the area was used for rotational production of vegetables such as cucumber (Cucumis sativus Linn.), cabbages (Brassica oleracea var. capitata) and tomatoes (Lycopersicon esculentum Mill.). The soil was

Conditions of simulated climate change

During the study period (12th August–11th November 2013), the temperature inside the greenhouses were on average 3.3 °C higher than the ambient temperature (Fig. 1b) and the soil moisture content was on average 14.4% lower than outside the greenhouse (Fig. 1c). The difference in soil moisture content between the greenhouse and non-greenhouse treatments fluctuated within a wider range during the first 21 days (6.25–53.57%, averaging 27.21%), after which the difference was kept at about 10.21% for

Discussion

A sound understanding on how projected climate change scenarios may impact on soil nitrifier and denitrifier communities and subsequent effects on N₂O emissions from vegetable soils is critically important for managing and minimizing the impacts of climate change. Results from this study clearly demonstrated that simulated temperature rise and drought conditions could affect both the population abundance and community structure of nitrifiers and denitrifiers in the vegetable soil, particularly

Conclusions

This study has clearly demonstrated that the effect of a projected climate change scenario on nitrifiers and denitrifiers and on N₂O emissions may be significantly magnified by the application N fertilizers, pointing to potentially major impacts on agricultural soils where N fertilizers are often applied. A projected future warmer and drier condition with N fertilizer use may lead to reduced N₂O emissions, and changed soil moisture content was shown to be the driving factor that controlled N₂O

Acknowledgments

This program was funded by Natural Science Foundation of China (41271272, 41301254, 41230857) and the National Key Basic Research Program of China (2014CB138801).

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Warmer and drier conditions alter the nitrifier and denitrifier communities and reduce N2O emissions in fertilized vegetable soils

Highlights

Abstract

Introduction

Section snippets

Site description

Conditions of simulated climate change

Discussion

Conclusions

Acknowledgments

Soil Biol. Biochem.

Appl. Soil Ecol.

Soil Biol. Biochem.

Soil Biol. Biochem.

Environ. Pollut.

Soil Biol. Biochem.

Soil Biol. Biochem.

Res. Microbiol.

Appl. Soil Ecol.

Atmos. Environ.

Soil Biol. Biochem.

Soil Biol. Biochem.

Atmos. Environ.

N2O emission rates in a California meadow soil are influenced by fertilizer level, soil moisture and the community structure of ammonia-oxidizing bacteria

Glob. Change Biol.

Alterations of nitrogen dynamics under elevated carbon dioxide in an intact Mojave Desert ecosystem: evidence from nitrogen-15 natural abundance

Oecologia

Influence of different cultivars on populations of ammonia-oxidizing bacteria in the root environment of rice

Appl. Environ. Microb.

Effects of multiple global change treatments on soil N2O fluxes

Biogeochemistry

Effects of climate change drivers on nitrous oxide fluxes in an upland temperate grassland

Ecosystems

Four years of experimental climate change modifies the microbial drivers of N2O fluxes in an upland grassland ecosystem

Glob. Change Biol.

Ammonia-oxidizing archaea: important players in paddy rhizosphere soil?

Environ. Microb.

Nitrous oxide emission factors for agricultural soils in Great Britain: the impact of soil water-filled pore space and other controlling variables

Glob. Change Biol.

Nitrous oxide emissions from intensive agricultural systems: variations between crops and seasons, key driving variables, and mean emission factors

J. Geophys. Res.

Environmental factors shaping the ecological niches of ammonia-oxidizing archaea

FEMS Microbiol. Rev.

Warmer and drier conditions alter the nitrifier and denitrifier communities and reduce N₂O emissions in fertilized vegetable soils

N₂O emission rates in a California meadow soil are influenced by fertilizer level, soil moisture and the community structure of ammonia-oxidizing bacteria

Effects of multiple global change treatments on soil N₂O fluxes

Four years of experimental climate change modifies the microbial drivers of N₂O fluxes in an upland grassland ecosystem