Global meta-analysis of terrestrial nitrous oxide emissions and associated functional genes under nitrogen addition

https://doi.org/10.1016/j.soilbio.2021.108523Get rights and content

Highlights

  • Nitrogen addition increased the abundance of AOA, AOB, nirK, nirS and nosZ.

  • N2O emission was negatively correlated with the abundance of nosZ gene.

  • N2O emission was positively correlated with the AOA and AOB abundance.

  • AOA, AOB and nosZ abundance were main factors affecting N2O emission.

  • Climate variables and available N concentrations were additional main factors.

Abstract

Functional genes involved in nitrogen (N) cycling regulate soil nitrification, denitrification and N2O emissions. However, the general patterns and variability of N functional genes in response to N addition, and their association with N2O emission have not been synthesized for terrestrial ecosystems. We synthesized 2068 observations from 144 papers to explore the impact of N addition on the abundance and diversity of N functional genes, and their relationship to N2O emissions in croplands, grasslands and forests on a global scale. In croplands, N addition increased N2O emissions (109%), the abundance of ammonia-oxidizing archaea (AOA) (19%), ammonia-oxidizing bacteria (AOB) (95%), nirK (52%), nirS (40%) and nosZ (41%), and the diversity of AOB (15%), nirS (12%) and nosZ (11%). In grassland, N addition increased AOB abundance (130%) and decreased the abundance of nirS (−99%) and nosZ (−58%) genes, but in forests, significant effects were only found for the abundance of AOA (35%) and AOB (121%). N2O emission was negatively correlated with the abundance of nosZ, but positively correlated with the abundance of AOA and AOB. Apart from the abundance of functional AOA, AOB and nosZ genes, climate variables (precipitation and temperature), and available N concentrations were the main factors explaining the variation in N2O emission with N addition, as shown by random forest analysis. These findings indicate that impacts on N functional genes that encode enzymes involved in nitrification (AOA, AOB) and in the transformation of N2O to N2 (nosZ) are the main mechanisms behind the effect on N fertilizer-induced N2O emissions.

Introduction

Nitrogen is an essential element that affects plant growth and productivity (Cole et al., 2016; Li et al., 2018). To meet the increasing food demands of the growing human population, N fertilizer inputs have increased rapidly over the past few decades (Lassaletta et al., 2014). These increased N fertilizer inputs have enhanced N2O emissions, with almost 60% of N2O being emitted from agricultural ecosystems (Soussana et al., 2007). N2O is the third most important greenhouse gas with a greenhouse effect 273 times greater than CO2 (IPCC, 2021), and it also depletes atmospheric ozone (Zhang et al., 2018). N2O emissions and its regulating mechanisms under enhanced N input have therefore received considerable attention over recent decades. Soil microorganisms are known as the primary drivers of nitrification and denitrification processes (Galloway et al., 2008; Canfield et al., 2010), and therefore affect N2O emission (Lam and Kuypers, 2011). To gain greater insight into the mechanisms responsible for N fertilizer-induced N2O emission, it is imperative for greater understanding of how soil microbial communities involved in soil N cycling respond to elevated N input.

Functional genes that encode soil N transformation enzymes are widely used as gene markers to represent nitrifiers and denitrifiers. Functional genes thus play a role in regulating N2O production processes by affecting the transformation of NH4+ to N2O in various steps from NH4+ to NO2, NO2 to NO, NO to N2O and N2O to N2. For example, archaeal and bacterial amoA genes are used as genetic markers for ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) (Francis et al., 2005; Jia and Conrad, 2009; Pester et al., 2012), being involved in the conversion of ammonia to nitrite (NO2) (Hu et al., 2015). In particular, nirS and nirK genes that encode nitrite reductase are used to indicate the denitrifiers converting NO2 to NO (Henry et al., 2004; Kandeler et al., 2006). The nosZ gene that encode nitrous oxide reductase catalyzes the transformation of N2O to N2, which is the final step of denitrification (Domeignoz-Horta et al., 2017). Understanding changes in the abundance and diversity of these N functional genes could give insight into the biotic mechanisms mediating N2O emissions.

A great number of publications have reported that anthropogenic N addition altered the abundance and diversity of N functional genes including amoA, nirK, nirS and nosZ in field experiments (Sun et al., 2015; Francioli et al., 2016; Wang et al., 2018). However, the response of functional genes to N addition varies, and appears to be affected by N application rate (Guo et al., 2017), N fertilizer type (i.e., organic fertilizer, inorganic fertilizer and organic-inorganic mixture) (Sun et al., 2015; Xiang et al., 2020), vegetation type (Azeem et al., 2020) and soil properties (Yuan et al., 2012). These impacts make it difficult to achieve a clear understanding on how N addition affects N functional genes and their relative contribution to N2O emission.

Recently, two meta-analyses examined the N addition effects on N functional genes, and reported that N fertilization increased AOA, AOB, nirK, nirS and nosZ abundance (Carey et al., 2016; Ouyang et al., 2018). However, Carey et al. (2016) only focused on the effect of N addition on amoA gene abundance involved in nitrification in managed and natural ecosystems; Ouyang et al. (2018) only did a meta-analysis of N functional genes (nifH, AOA, AOB, nirS, nirK and nosZ) in response to N fertilization in agricultural ecosystems with nifH being a gene encoding enzymes involved in the fixation of atmospheric N2 into a form of N available to living organisms. These two studies were limited by focusing on impacts on the abundance of N functional genes only, not considering the impacts on functional gene diversity, nor simultaneously accounting for the impact of N2O emissions. Furthermore, the meta-analyses of Ouyang et al. (2018) was limited to agricultural land. The effect of N addition on N functional genes involved in nitrification and denitrification might be different in grasslands and forests as compared to croplands because of the lower anthropogenic disturbance in grasslands and forests (Jangid et al., 2008; Chen et al., 2019a). Given the diversity of biome types and edaphic conditions across individual site-based studies, it is of vital importance to synthesize the response of N functional gene diversity to N addition in terrestrial ecosystems on a global scale.

Although there are many studies reporting the regulatory factors associated with N2O emissions (Cai et al., 2010; Soares et al., 2016; Domeignoz-Horta et al., 2017; Fan and Yoh, 2020), there is no consistent conclusion on the relative contribution of functional genes and environmental factors to N2O emissions in response to N addition. For instance, Soares et al. (2016) found that N2O emissions were correlated with bacterial amoA abundance, but not with the abundance of nirK, nirS and nosZ in soil fertilized with different N sources, indicating that AOB might be the main contributor to N2O emissions. However, Domeignoz-Horta et al. (2017) analyzed more than 59,000 field measurements and found that the diversity of the nosZ was most important for explaining the variation of N2O emissions in situ. Apart from the abundance of different N functional genes, climate variables, such as precipitation, temperature and soil moisture are also factors explaining the variation in N2O emissions. For example, Li et al. (2019) investigated the effect of global climate change on N2O emissions and the related N functional genes in terrestrial ecosystems, and found that precipitation promoted N2O emissions by 55% while lower precipitation rates inhibited N2O emissions by 31%, and the effects size of precipitation changes to nosZ and nirS abundance/diversity had a U-shaped relationship with soil moisture. At the same time, N2O emission was positively related with soil moisture (Li et al., 2019), highlighting the importance of environmental factors in driving N2O emission. However, to date, there has been no synthesis of how N addition concurrently affects the soil N functional gene abundance, diversity and N2O emission, limiting our understanding of the associations between N2O emissions and N functional genes. There is a need to synthesize available data to identify the biotic mechanisms responsible for N2O emissions under N addition on a global scale.

More specifically, we lack insight in the relative contribution of N functional genes to N2O emission by encoding enzymes involved in the transformation of NH4+ to NO2 (AOA, AOB), NO2 to N2O (nirS and nirK) and N2O to N2 (nosZ).To address the lack of understanding of how N addition alters N functional genes and N2O emissions from terrestrial ecosystems, we collected 2068 observational data from 144 field studies to quantitatively synthesize N functional gene abundance and diversity, and the relevant N2O emissions and N-cycling processes under N additions. We hypothesized that N addition affects all genes involved in N2O production (AOA, AOB, nirS and nirK) and N2O consumption (nosZ) in a comparable way. We aimed (1) to identify the response of N functional gene abundance and diversity, and the associated N2O emissions, N-cycling processes and soil properties to N addition; (2) to relate the variation in the response between studies to N addition rate, form and different biomes; and (3) to explore the abiotic (climatic and edaphic factors) and biotic (N functional gene) factors driving the changes in N2O emissions under N addition.

Section snippets

Data collection

In order to study the effects of N addition on N functional genes, we collected data from papers that were published between 1991 and 2020 using Web of Science (https://www.webofscience.com) and China National Knowledge Infrastructure (https://www.cnki.net) databases using the search term, "TS = (AOA OR archaeal amoA OR AOB OR bacterial amoA OR nirS OR nirK OR nosZ) AND (nitrogen addition OR nitrogen fertilization OR nitrogen deposition OR nitrogen application OR nitrogen enrichment)" for

Effect of N addition on N2O emissions, N-cycling processes and soil properties

A summary of the means and ranges of effect sizes with respect to N addition on PNR, PDR and N2O emissions and soil properties is given in Fig. 2, Fig. 3 and Table S4. Across all studies, N application increased PNR on average by 68%, PDR by 40% and N2O emissions by 121% (Fig. 2). N addition increased N2O emissions in both croplands and grasslands, but data were lacking for forests. However, while N addition increased the effect size of PNR in all ecosystems significantly (P < 0.05), the effect

Impacts of N addition on the abundance and diversity of N functional genes

The N functional gene abundance was found to be more sensitive to N addition in croplands than in natural grasslands and forests. We also found AOB, nirS and nosZ diversity were more responsive in agricultural ecosystem than in natural ecosystems. The variation in N functional gene abundance and diversity may be due to differences in the intensity of anthropogenic disturbance. Compared to natural ecosystems, the higher anthropogenic disturbance in agricultural ecosystems affects soil

Conclusion and implications

Our meta-analysis provides three important insights into the role of N functional genes in regulating N2O emission. Firstly, impact of N addition on N-cycling genes clearly differs among croplands, grasslands and forests. Where N addition increased the abundance of all N functional genes as well as the diversity of AOB, nirS and nosZ in croplands, effects varied in grasslands and forests. In grassland, N addition significantly affected the abundance of AOB, nirS and nosZ, but in forests,

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

We thank Qi Shao and Shenglei Hao for data collection and proofreading on the manuscript. This work was financially supported by National Natural Science Foundation of China (41877046), the Second Tibetan Plateau Scientific Expedition and Research (STEP) program (2019QZKK0308) and China Scholarship Council (No.201913043).

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