Plants with an ammonium preference affect soil N transformations to optimize their N acquisition

Highlights

• Significant interactions between plants and soil N transformations were observed.

• NH₄⁺-preferring plants outcompeted microbes for NH₄⁺.

• Soil microorganisms switched to assimilate NO₃⁻ in the presence of NH₄⁺-preferring plants.

• Plants preferring NH₄⁺ can induce heterotrophic nitrification.

Abstract

Our understanding of how plants influence the gross rates of specific soil N transformations in plant-soil systems is still rudimentary, providing the incentive for our current study. A ¹⁵N tracing study was carried out with plants known for their NH₄⁺-preference to quantify the gross soil N transformation and gross plant N uptake rates. Significant interactions between plants and gross rates of soil N transformations were observed. The rates of NH₄⁺ uptake by sugarcane (3.74 mg N kg⁻¹ d⁻¹) and tea (3.34 mg N kg⁻¹ d⁻¹) were much higher than microbial NH₄⁺ immobilization rates (0.01, and 0.27 mg N kg⁻¹ d⁻¹, respectively), suggesting that NH₄⁺-preferring plants outcompeted microbial NH₄⁺ acquisition. The gross rates of NO₃⁻ immobilization increased with decreasing gross NH₄⁺ immobilization rates, indicating a switch towards microbial NO₃⁻ uptake under high plant NH₄⁺ demand. Moreover, the gross rates of autotrophic nitrification, the classical NO₃⁻ production pathway, was generally low in the studied acidic soil (average 0.40 mg N kg⁻¹ d⁻¹ in plant treatments), and was insufficient to meet the total NO₃⁻ demand (average 2.37 mg N kg⁻¹ d⁻¹). Gross rates of heterotrophic nitrification, ranging from 0.31 to 0.57 mg N kg⁻¹ d⁻¹, were stimulated by the presence of plants and were generally responsible for 49–69% of total NO₃⁻ production in the plant treatments, while this rate was negligible in the absence of plant. Heterotrophic nitrification might provide additional NO₃⁻ to meet N requirements of plants and microorganisms. This is supported by the positive correlation of gross heterotrophic nitrification coupled with gross NO₃⁻ immobilization and plant N uptake rates. Interactions between plant N acquisition and soil N transformations exist and plant-soil studies are key to identify feedbacks between plants and soil microbes.

Introduction

Nitrogen (N) is an essential element for maintaining life in the biosphere and is often the limiting element for ecosystem productivity. Thus, strong N retention strategies, such as low NH₄⁺ oxidation rates, efficient NO₃⁻ immobilization into organic N, and dissimilatory nitrate reduction to ammonium (DNRA), are critical for the fertility for instance of humid forest soils (Stark and Hart, 1997; Huygens et al., 2008; Zhang et al., 2013). Besides the available N retention capacities, the interactions between plants and soil microbes can also affect plant N acquisition (Song et al., 2007; Inselsbacher et al., 2010; Blagodatskaya et al., 2014). Generally, there is a strong competition for N between microbes and plants (Harrison et al., 2008; Inselsbacher et al., 2010) and plants have evolved different N nutritional strategies to optimize N acquisition under various growing conditions (Ehrenfeld et al., 2005; Hu et al., 2018). Previous studies have focused on the competition between microbial N immobilization and plant N acquisition, the chemical N forms and plant N uptake, plant-mediated effects on net N mineralization and nitrification rates (Ehrenfeld et al., 2005; Jackson and Cavagnaro, 2008; Nacry et al., 2013; Zhang et al., 2016c). However, most of these studies did not quantify the interactions between plants and soil microbes but focused only on the net transformation dynamics. Thus, a quantitative understanding based on plant N acquisition and soil gross N transformations in the plant-soil systems is largely lacking.

With the rapid development of ¹⁵N-tracing technology, new approaches are now available to simultaneously quantify the gross rates of soil N transformation and plant N uptake in plant-soil systems (Inselsbacher et al., 2013; He et al., 2020). A recent study using the ¹⁵N tracing tool Ntrace_plant found that gross rates of heterotrophic nitrification and NO₃⁻ immobilization were significantly higher in subtropical acidic soil planted with sugarcane (an NH₄⁺-preferring plant) than in the control soil (without plant) while NH₄⁺ immobilization rates were significantly lower compared to the control (He et al., 2020). Thus, it seems that at least plants with a preference for NH₄⁺ are able to outcompete soil microorganisms for NH₄⁺ and provide a pressure for microorganisms to utilize NO₃⁻ to meet their N requirements. The generally low autotrophic nitrification rates in acidic soils also explain the dominance of NH₄⁺ in soil mineral N for plant N uptake (Zhang et al., 2018). Thus, the stimulation of heterotrophic nitrification by plants is likely to be a strategy to meet NO₃⁻ requirement of both plants and microorganisms. An increasing number of studies have found that heterotrophic nitrification occurs more widely than previously thought, and may even be the dominant pathway of NO₃⁻ production in acidic, humid forest soils (Huygens et al., 2008; Zhang et al., 2015, 2018). The large amount of NO₃⁻ generated via heterotrophic nitrification in acidic, humid forest soils, appears to contrast with the N retention strategy, especially for humid ecosystems. Plants growing in acidic soils, such as Dicranopteris linearis (Xu et al., 2014), Pinus massoniana Lamb (Zhang et al., 2019b), Camellia sinensis (Ruan et al., 2007), and Saccharum officinarum (Nastaro et al., 2018) prefer NH₄⁺ uptake. Moreover, it has also been reported that NO₃⁻ immobilization is a widespread process in acidic, humid subtropical forest soils, despite the fact that microbes generally prefer NH₄⁺ as N source (Cresswell and Syrett, 1979; Rice and Tiedje, 1989; Zhang et al., 2011, 2013). These interactions between plant N acquisition, microbes N immobilization and soil N transformations are likely to provide N nutritional strategies for plants and soil microbes to alleviate the N competition in the plant-soil systems (Ehrenfeld et al., 2005). However, very few investigations have focused on simultaneously quantifying the gross rates of soil N transformation and plant N uptake in the plant-soil systems to identify relationships between plants and microbes with respect to their N demand.

Thus, we hypothesize that plant N acquisition capacities affect the specific soil N transformations to meet N demands of plants and soil microorganisms. Specifically, the NH₄⁺ preference plants compete strongly with soil microorganisms for NH₄⁺, providing a pressure for microorganisms to switch to a predominant microbial NO₃⁻ assimilation. To meet the NO₃⁻ demand in acidic soils, heterotrophic nitrification is stimulated in presence of plants due to the small autotrophic nitrification rate in these soils. To test our hypotheses, a series of ¹⁵N-tracing pot experiments were carried out with NH₄⁺-preferring plants with different N acquisition capacities.