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Article

Straw Returning Alleviates the Inhibition of Soil Nitrification Medicated by Ammonia-Oxidizing Archaea under Low Nitrogen Fertilization

by
Feng Wang
1,
Xiaolong Liang
2,
Minjie Liang
1,
Bingqing Guo
1,
Shuangyi Li
1,
Lingzhi Liu
1,* and
Jingkuan Wang
1,*
1
Key Laboratory of Arable Land Conservation in Northeast China, Ministry of Agriculture and Rural Affairs, College of Land and Environment, Shenyang Agricultural University, No. 120 Dongling Road, Shenhe District, Shenyang 110086, China
2
Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(7), 1550; https://doi.org/10.3390/agronomy14071550
Submission received: 3 June 2024 / Revised: 8 July 2024 / Accepted: 15 July 2024 / Published: 17 July 2024
(This article belongs to the Special Issue Keeping Nutrients in the Soil: The Challenges, Benefits and Trade-Offs)
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Versions Notes

Abstract

:
Straw returning may stimulate soil microbial activity, thereby influencing microbial-mediated soil nitrification, which can lead to nitrate leaching and nitrogen (N) loss. However, its effects under long-term nitrogen fertilization remain unclear. At an experimental station with 34 years of fertilizer application (0, 135, and 270 kg ha−1 N), we investigated how nitrogen fertilization and straw returning affected the soil potential nitrification rate (PNR) and ammonia-oxidizing microorganisms (AOM). Our results suggest that N fertilization concurrently inhibits soil PNR, but this inhibition can be alleviated by straw returning, particularly with low nitrogen fertilization (p < 0.05). Long-term N fertilization significantly decreased the abundance of ammonia-oxidizing archaea (AOA), ammonia-oxidizing bacteria (AOB), and complete ammonia-oxidizing bacteria cladeB (CAOB-cladeB). Straw returning increased AOA abundance and diversity, especially with low or no fertilization (p < 0.05). Furthermore, the partial least squares path model demonstrated that AOA abundance affected soil PNR by altering the AOA community. According to random forest analysis, soil pH and AOA beta diversity were the primary factors affecting soil PNR (explaining 10.76% and 10.03% of the variation, respectively). Overall, our findings highlight the importance of straw returning and AOA in soil nitrification under long-term nitrogen fertilization, emphasizing the need to consider these interactions for sustainable agriculture.

1. Introduction

Nitrification is the process by which ammonia (NH4+) is transformed into nitrate (NO3−), mediated by ammonia-oxidizing archaea (AOA), ammonia-oxidizing bacteria (AOB), and complete ammonia-oxidizing bacteria (CAOB) [1,2,3]. Microbial nitrification, the only biological process connecting the oxidation and reduction of inorganic nitrogen (N) pools, has been extensively studied over the past two decades due to its foundational role in nutrient cycling and environmental sustainability [4,5]. This process in agriculture is crucial for soil fertility, regulating plant nitrogen utilization, and maintaining ecosystem balance [6,7].
Anthropogenic activities, notably the widespread application of nitrogen fertilization, have profoundly impacted soil nitrification dynamics, raising concerns about nitrogen loss, greenhouse gas emissions, and ecosystem pollution [8]. While nitrogen fertilization may enhance crop yield under certain conditions, it can also lead to nitrogen loss through leaching, denitrification, and nitrous oxide (N2O) emissions, the latter being a potent greenhouse gas [9].
Soil nitrification responses to nitrogen fertilization are complex and diverse, depending on various factors such as soil properties and environmental conditions that lead to change of the functional microbial community [10]. For instance, alkaline soils may exhibit increased gross nitrification rates following nitrogen fertilization application [11,12], while acidic and neutral soils may experience inhibition due to ammonium toxicity [13]. The composition and abundance of nitrification microorganisms, especially AOA, AOB, and CAOB, exert significant control over soil nitrification potential and nitrogen utilization efficiency [7]. These microorganisms have unique physiological characteristics, occupy specific ecological niches, and exhibit different responses to environmental changes, thereby influencing their contributions to soil nitrification [14,15,16,17]. CAOB usually dominates in barren environments due to its strong affinity to ammonia [18], but it may not be the predominant nitrifier in soils with high N fertilization levels. Therefore, in representative farmlands of China, the CAOB abundance was lowest in all treatments [19]. Generally, AOB tends to be sensitive to the influence of inorganic N fertilizers, such as urea fertilizer [20], whereas AOA can be affected by organic amendments or co-application with chemical fertilizer [21]. However, previous studies revealed that AOA is more sensitive in acidic conditions and contributes more than AOB, despite AOB being more adaptable to high ammonia conditions [22,23].
Additionally, organic amendments such as straw residues, biochar, and manure have been identified as potential strategies to alleviate the inhibitory effects of nitrogen fertilization on soil nitrification by providing energy and modulating microbial community structure [13,24,25]. Straw decomposition serves as a major source of organic carbon and nutrients [26,27], regulating soil nitrification dynamics by altering functional microbial activity and the balance of carbon and nitrogen [28,29]. However, the effect of straw returning on soil nitrification and related microorganisms is influenced by the fertilization regime [30]. Chen et al. [31] demonstrated that the AOB community responded more sensitively to straw returning combined with N fertilization than AOA in alkaline purple soil. However, in acid paddy soil, straw returning can enhance the diversity of the AOA community and AOA had a closer association than AOB with potential nitrification activity [32]. In acidic tropical vegetable soil, straw returning has been shown to increase the nitrification potential by stimulating the AOA abundance [33]. Furthermore, the co-application of straw returning and N fertilization in neutral paddy soil significantly increased the amoA gene abundance of both AOA and AOB, with AOA showing more sensitivity to the treatments than AOB [34]. These findings underscore the significance of AOA in acidic agricultural soils and emphasize the intricate relationships among nitrogen fertilization, straw return, microbial communities (especially AOA), and soil nitrification dynamics. A comprehensive analysis is urgently required to elucidate these relationships and enhance our understanding of soil nitrogen cycling mechanisms.
Here, we examined how straw returning affects the nitrifying microorganisms in a fertilization station and evaluated their contribution to nitrification. We hypothesized that (1) straw returning would enhance soil nitrification under N fertilization, (2) the abundance of AOA would primarily positively contribute to soil nitrification, and (3) soil pH would regulate soil microbial nitrification dynamics by altering the AOA community.

2. Materials and Methods

2.1. Experimental Site and Design

The experimental station (41°49′ N, 123°34′ E), with a mean annual precipitation of 705 mm and a mean annual temperature of 7.9 °C, was initiated in 1987 and located at Shenyang Agricultural University, Shenyang City, China. The experimental site was cultivated with maize monoculture (early May to early October), followed by winter fallow. The soil used for the field trials is classified as an Alfisol [35].
This study included six treatments as follows: (i) unfertilized control (N0), (ii) 135 kg N ha−1 yr−1 urea chemical fertilizer (N135), (iii) 270 kg N ha−1 yr−1 urea chemical fertilizer (N270), (iv) unfertilized control plus straw residue of maize (N0 + S), (v) urea chemical fertilizer (N135) plus straw residue of maize (N135 + S), and (vi) urea chemical fertilizer (N270) plus straw residue of maize (N270 + S). The plot size of each treatment was 69 m2, arranged in a randomized block design. Over the past 34 years, at the experimental station, all fertilizers in each treatment were applied once as basal fertilizer each April. Table 1 shows the basic properties of the tested soil before straw returning. Soil samples from each fertilization treatment were collected at the 0–20 cm soil depth, where soil microbial activity is most vigorous, using an auger before maize planting in April 2021. Five soil cores (approximately 5 cm in diameter) were taken from each plot and were thoroughly mixed to form a composite sample per replicate plot. Each soil core was manually broken apart along the natural break points and sieved (<2 mm) to remove the non-soil components such as visible rocks and litter. Subsequently, the composite samples were mixed with or without maize straw residues (≤1 cm) and then put into nylon bags (50 μm mesh size) with three replicates. The addition rate of straw residue corresponded to 1% of the weight of the air-dried soil weight (i.e., 2 g of straw residue added to 200 g of air-dried soil), with three replicates of each treatment. The organic carbon content of the tested straw residues was 387 g kg−1, and the total nitrogen content 13.01 g kg−1. The nylon bags from six treatments were then buried back in the original plot at 0–20 cm depth on 24 June 2021, retrieved after 30 days, and transported to the laboratory on ice. The undecomposed straw residues were manually picked out of the nylon bags using tweezers, and the tested soils were stored at −80 °C.

2.2. Straw Decomposition Proportion and the Activity of Cellulase and Xylanase Determination

The undecomposed straw residues were washed with deionized water, and the mass of the straw residues was determined after being dried at 60 ℃ for 24 h. Then, the percentage of the weight of decomposed straw to its original weight was used to reflect the straw decomposition proportion [36].
The activities of cellulase and xylanase were determined using 3,5-dinitrosalicylic acid (DNS) [37,38]. Briefly, fresh soil (10.0 g) was placed in a 50 mL conical flask, followed by addition of 20 mL of 1% carboxymethyl cellulose solution (or 1% xylan solution), 5 mL of pH 5.5 phosphate buffer, and 1.5 mL of toluene. The flask was then incubated at 37 °C for 72 h. After incubation, 1 mL of filtrate was transferred to a 25 mL flask, followed by addition of 3 mL of 3,5-dinitrosalicylic acid solution. The mixture was boiled in a water bath for 5 min, rapidly cooled for 3 min, brought up to volume to 25 mL, and left to stand for 5 min before colorimetric measurement at 540 nm. The activity of cellulase (xylanase) was determined by the amount of enzyme needed to hydrolyze cellulose (xylan) per gram of dry soil per hour.

2.3. Soil Properties and Potential Nitrification Rate Determination

The soil pH was determined using a soil-to-water ratio of 1:2.5. The mixture was shaken for 30 min, allowed to settle, and then the pH was measured using a pH meter with a glass electrode (Metrohm 702, Herisau, Switzerland). The determinations of the soil organic carbon (SOC) and total nitrogen (TN) contents used a Vario EL III elemental analyzer (Elementar, Langenselbold, Germany). The concentrations of ammonium nitrogen (NH4+-N) and nitrate nitrogen (NO3−-N) were extracted by 2M KCl and measured by a continuous flow analyzer (Auto-Analyzer III-HR, Norderstedt, Germany), respectively.
The method for determining soil potential nitrification rate (PNR) was the same as previously described [39]. Briefly, 5.0 g fresh soil sample was placed in a 50 mL conical flask, followed by addition of 1 M phosphate buffer solution with 1.5 mM (NH4)2SO4. The flasks were incubated at 25 °C in darkness for 14 days. After incubation, 25 mL of 1 M KCl solution was added to each flask, and the nitrate (NO3−-N) concentrations in the supernatant were measured immediately. The PNR was calculated based on the amount of NO3−-N produced per kilogram of dry soil per unit time.

2.4. Quantification of amoA Genes

The total DNA was extracted from soil samples using a Soil DNA Kit (Omega Bio-tek, Norcross, GA, USA). The concentration, quality, and purity of DNA were detected by using an ND-2000 spectrophotometer (NanoDrop, Wilmington, DE, USA) and agarose gel electrophoresis.
To quantify the abundances of AOA, AOB, and CAOB, DNA-based qPCR with three technical replicates was performed using an ABI StepOne Plus PCR System (Applied Biosystems, Waltham, MA, USA) and their corresponding specific primer set (Table S1) [2,40,41]. The 20 μL reaction system contained 10 μL Ultra SYBR Mixture (CWBIO, Taizhou, China), 2 μL DNA template, and 0.8 μL primers (10 μM). Deionized water as a negative control was used to ensure all reagents were without contaminants. The amplification efficiencies and R2 values of all detected genes were greater than 80% and 0.99, respectively.

2.5. Amplicon Sequencing

The sequences of the AOA amoA gene were amplified by PCR and purified by a DNA Gel Extraction Kit (Axygen Biosciences, Union, CA, USA). A Quantus™ Fluorometer (Promega, Madison, WI, USA) was used to detect and quantify the purified products. The DNA library was built and further sequenced using the NEXTFLEX® Rapid DNA-Seq Kit and Illumina’s Miseq PE300 platform (Majorbio, Shanghai, China), respectively.
QIIME 1.9.1. and Uparse 11 were used for the assembly and cluster of DNA sequences, and the similarity threshold of 97% was regarded as an operational taxonomic unit (OTU). The raw sequences were uploaded to the NCBI with the accession number PRJNA985879.

2.6. Data Analysis

A one-way analysis of variance (ANOVA), followed by an LSD test, was used to compare variable means of straw decomposition proportions among different N fertilizer application rates using IBM SPSS 20.0. A two-way ANOVA was performed with N fertilizer application rates and straw application rates as the main factors for each variable using the car package in R 4.1.1. Simple linear regression was used to reflect the relationship between PNR and amoA gene abundance and the dominant AOA phylogenetic clades. Mothur 1.30.2 was used to calculate the community diversity indices at the OTU level. The a-diversity of AOA community was assessed using the Chao1, Shannon, and Simpson indices. MEGA-X was used to construct a neighbor-joining tree (P-distance model) to perform the community phylogenetic analysis [42]. The vegan package in R 4.1.1 was used for the principal coordinate analysis (PCoA) and distance-based redundancy analysis (db-RDA) to visualize the community’s differences and their correlation with soil properties, and the variables in db-RDA were interpreted using the data.hp package in R 4.1.1 [43].
A partial least square path model (PLS-PM) analysis was used to evaluate the effects of various factors, including N fertilization and straw application rates, straw decomposition (including cellulase and xylanase activity), soil properties (including soil pH, C/N ratio, NH4+/NO3− ratio, and the content of SOC, TN, NH4+, NO3−), AOA abundance, and AOA amoA community (including PCoA1 of the AOA community and sequences of AOA-Clade A, AOA-Clade B, and AOA-Clade Nitrososphaera), on soil PNR. The model was constructed using the PLSPM package in R 4.1.1, and a larger GoF index indicated a better model fit in this model [44]. The randomForest, A3, and rfPermute packages in R 4.1.1were used to perform the random forest (RF) analysis and investigate the model and variables’ significance level to evaluate the importance of individual variables that affect soil PNR.

3. Results

3.1. Straw Decomposition and Potential Nitrification Rate

N fertilization application promoted straw decomposition as we observed an average increase of 38.89% and 22.22% in the N135 + S and N270 + S treatments, respectively, relative to the N0 + S treatment in the proportion of straw decomposition (p < 0.05; Figure 1A). Independent and combined N fertilization and straw returning can increase the activities of cellulase and xylanase (p < 0.05; Figure S1; Table S2). The difference in cellulase activity between samples with and without straw addition is greater for N0 treatment (with a growth rate of 65.71%) than for N135 and N270 treatments (with a growth rate of −0.87% and 9.96%, respectively). However, the variance in xylanase activity is more pronounced for N135 treatment (with a growth rate of 16.75%) than for N0 and N270 treatments (with a growth rate of 4.05% and 7.65%, respectively).
Long-term N fertilization clearly inhibited the soil PNR (p < 0.01; Figure 1B; Table S2). Compared to the control treatment (N0), PNR decreased by 53.34% and 63.70% in the N135 and N270 treatments, respectively. The incorporation of straw can mitigate the inhibitory effect of nitrogen fertilization on PNR, and this effect was observed significantly in the N135 + S treatment, which showed a 31.18% increase relative to the N135 treatment. In contrast, the N270 + S treatment did not exhibit a significant effect on PNR.

3.2. Soil Properties

Both independent and combined N fertilization application and straw returning significantly influenced the soil properties (p < 0.01; Table S2). Independent application of N fertilization decreased soil pH and SOC content, whereas straw returning could markedly alleviate soil acidification and decline in SOC content (p < 0.05; Table 2). The SOC content in the N135 + S treatment significantly increased by 9.24% compared to the N135 treatment, and the soil pH increased from 4.96 in the N270 treatment to 6.05 in the N270 + S treatment.
In comparison to the N0 treatment, the contents of TN, NH4+-N, and NO3−-N increased significantly in the N135 and N270 treatments (p < 0.05), and straw returning positively impacted these soil properties as well. In the N135 + S treatment, the concentrations of NH4+-N and NO3−-N increased by 43.60% and 161.54%, respectively, relative to the N135 treatment. However, in the N270 + S treatment, the concentrations of NH4+-N and NO3−-N increased by 72.97% and 15.26%, respectively, relative to the N270 treatment (p < 0.05; Table S2).

3.3. Quantification of amoA Gene

The interaction between fertilization and straw returning had no significant effect on the abundance of soil nitrification microorganisms (Table S2). Long-term N fertilization significantly inhibited AOA amoA abundance (Figure 2; p < 0.05). The abundance of AOA decreased by 26.88% and 21.51% in the N135 and N270 treatments compared to the N0 treatment, respectively. Similarly, compared to the N0 + S treatment, the abundance of AOA decreased by 21.74% and 24.92% in the N135 + S and N270 + S treatments, respectively. However, no significant difference was observed between the high and low N fertilization level. The response of AOB and CAOB-cladeB abundance to fertilization was similar to that of AOA (Figure S2A,C), whereas CAOB-cladeA exhibited an opposite trend (Figure S2B). N fertilization increased the abundance of CAOB-cladeA, particularly at the high N level (N270 and N270 + S treatments) (p < 0.05).
The application of straw significantly affected only the AOA amoA abundance (p < 0.05), but other tested microorganisms (AOB and CAOB) were not clearly influenced by straw returning (Table S2). The AOA abundance was clearly higher in the N0 + S and N135 + S relative to the N0 and N135 treatments, respectively (Figure 2; p < 0.05), and this corresponded with the trend of soil PNR.

3.4. Amplicon Sequencing of Ammonia-Oxidizing Archaea

The application of independent N fertilization evidently changed the α-diversity indices of the AOA community (Table S3). More precisely, fertilization could decrease the Shannon index but increased the Simpson index, thereby among all fertilization treatments, the N135 treatment had the lowest Shannon and highest Simpson indices (p < 0.05). However, the Chao1 index showed no clear difference between different treatments. Straw returning can increase the diversity of the AOA community under low N fertilization. The N135 + S treatment had a higher Shannon index and a lower Simpson index relative to the N135 treatment (p < 0.05), but straw returning had less influence on the N0 + S and N270 + S treatments (Table S3).
The most dominant OTUs of the AOA community, with a relative abundance of over 1%, belong to Thaumarchaeota Group I.1b. The AOA communities were composed of three distinct phylogenetic clades: AOA-Clade A, AOA-Clade B, and AOA-Clade Nitrososphaera (Figure S3). In the treatments without N fertilization, AOA-Clade A was dominant with a relative abundance of 59% in the N0 treatment and 58% in the N0 + S treatment. But with low and high N fertilization, the relative abundance of AOA-Clade A significantly decreased, and the relative abundance of AOA-Clade B and AOA-Clade Nitrososphaera clearly increased (p < 0.05). AOA-Clade B, with a relative abundance of 49–51%, was more abundant than AOA-Clade A and AOA-Clade Nitrososphaera in the N135, N135 + S, N270, and N270 + S treatments (Figure 3A). Furthermore, straw returning could not change significantly the relative abundance of AOA-Clade A, AOA-Clade B, and AOA-Clade Nitrososphaera. The result of PCoA also revealed that the AOA community’s beta diversity showed significant differences among the treatments of no, low, and high N fertilization, but had non-significant differences between the treatments applied or without straw (Figure 3B). These results emphasize the importance of N fertilization in the AOA community.

3.5. Impacts of Various Factors on Ammonia-Oxidizing Archaea and Potential Nitrification Rate

The effect of soil properties on the AOA community was demonstrated by db-RDA (Figure 4). The cumulative contribution of variance of soil properties to the AOA community was 93.59% for the first two axes, and the first constrained ordination axis (CPA1) explained most of the variation (79.09%). The NH4+/NO3− ratio was mostly associated with the AOA community, with an individual explanation of 17.13%, followed by the N fertilizer application rates, soil C/N ratio, pH, and cellulase activity, with explanations ranging from 11.16% to 16.42% (Table S4).
The partial least squares path modeling (PLS-PM) was constructed to demonstrate the effects of various factors on soil PNR (Figure 5). The N fertilizer application rates, soil properties, and the AOA amoA community directly affected soil PNR (p < 0.05). Regression analysis further revealed the positive correlation of the sequences of the AOA-Clade A with soil PNR and the negative correlation of the sequences of AOA-Clade B and AOA-Clade Nitrososphaera with soil PNR (Figure S4A–C; p < 0.05). Although no significant direct effects were found, the positive indirect effect of the straw application rates and straw decomposition on soil PNR through changing soil properties can be observed (Table S5).
The individual importance of each variable for soil PNR was demonstrated using random forest analysis (Table S6; R2 = 0.85; p < 0.001). Soil pH showed the highest predictive potential for soil nitrification, followed by beta diversity of the AOA community (PCoA1), N fertilizer application rates, and soil C/N.

4. Discussion

4.1. Soil PNR and Nitrifying Microorganism Abundance under Long-Term N Fertilization and Straw Returning

N fertilization has a direct impact on the concentrations and proportion of available nitrogen, consequently influencing soil nitrification [39]. Additionally, when straw is returned to the soil, it releases abundant nutrients, potentially enhancing the efficiency of N fertilizer utilization and altering soil nitrification by regulating nutrient availability such as the C/N ratio [45]. This highlights the intricate relationship between N management, organic matter inputs, and nutrient dynamics in agricultural systems. Variations in nitrification rates can reflect the transformation of available nitrogen in the soils. Although increased nitrification rates may lead to nitrate leaching, they also enhance soil nitrate content. Conversely, low nitrification rates may result in insufficient soil nitrogen supply, limiting crop growth [46]. This study revealed a notable decline in soil potential nitrification rates (PNR) ranging from 53.39% to 74.05% with increasing N fertilization rate (Figure 1B; p < 0.05). However, the application of straw significantly increased soil PNR in treatments without N fertilization (N0 + S) and with low N fertilization application (N135 + S). Compared to treatments without straw, soil PNR in N0 + S and N135 + S treatments increased by 29.97% and 31.18%, respectively. This finding is in agreement with a previous report indicating that rice straw returning positively influenced soil nitrification potential in paddy soil [47]. Although the high moisture and anaerobic conditions of paddy soils differ significantly from the conditions in our study, the increase in soil organic carbon and the impact on nitrification after straw returning showed similar trends in both environments. But in this study, this enhanced effect of straw was not observed in the treatment with higher N fertilization levels (N270 + S) (Figure 1B). This might be due to the considerable alteration of soil pH in the N270 + S treatment, in contrast to the N0 + S and N135 + S treatments, which would make it difficult for the original nitrifying microorganisms to adapt [48,49]. Another possible reason could be the incomplete decomposition of straw returning, which might result in a lower impact of straw returning on soil PNR compared to N fertilization (Figure 2A).
Fertilization also had a stronger impact than straw returning on the abundance of nitrifying microorganisms. The abundance of AOA, AOB, and CAOB-cladeB was reduced in the N fertilization (N135 and N270) treatments (Figure 2; Figure S2). Previous studies showed similar results in acidic habitats, suggesting that N fertilization can inhibit soil nitrification [21,50]. Compared to AOA, AOB, and CAOB-cladeB, the abundance of CAOB-cladeA was clearly increased in the high N fertilization (N270 and N270 + S) treatments (Figure S2B). Due to the relatively high substrate affinity of CAOB, it has been commonly believed that CAOB would be more suited to low ammonia concentrations [51]. However, recent studies have suggested that CAOB-cladeA may have a competitive advantage in high ammonia conditions due to its special AMO enzymes [52,53]. Furthermore, our findings can support the view that CAOB-cladeA has less contribution to agricultural soil nitrification because of its relatively lower abundance and negative correlation with soil nitrification [18], despite CAOB-cladeA having a positive response to N fertilization. Straw returning only increased the AOA amoA gene abundance but not that of other nitrifying microorganisms (Figure 2). This result, combined with the similar response of soil PNR and AOA abundance to N fertilization (Figure 1 and Figure 2), supported the notion that AOA may be the primary driver of soil nitrification. This observation is consistent with findings from Tzanakakis et al. [13], who suggested that potential nitrification activity derived from AOA increased in treatments with added N fertilizer and straw residue, while potential nitrification activity derived from AOB declined. The positive response of the AOA abundance to straw returning may be attributed to its unique mixotrophic nature [54,55]. Previous research, both in field and pure cultures, had validated that organic compounds could stimulate AOA growth [56,57]. Another viewpoint suggested that the addition of organic matter was reported to enhance AOA growth by reducing oxidative stress [58].
Overall, straw returning did not alter the inhibitory trend of soil PNR and the abundance of nitrifying microorganisms by N fertilization, compared to samples without fertilization (Figure 1 and Figure 2). While the impact of straw returning on soil nitrification may be limited, its promoting role under low N fertilization cannot be ignored. This highlights the importance of considering both straw returning and nitrogen fertilization strategies in agricultural management practices to optimize soil nutrient dynamics and minimize environmental impacts.

4.2. Ammonia-Oxidizing Archaea Community under Long-Term Nitrogen Fertilization and Straw Returning

The significance of AOA in soil nitrification and its close relationship with straw residues in our study necessitated an examination of the disparities between the AOA community under straw returning and N fertilization. In our community analysis based on the AOA amoA gene, the relative abundance of its phylogenetic clades was notably influenced by N fertilization rather than straw returning (Figure 3). AOA-Clade A, the most prevalent phylogenetic clade in AOA according to Bates et al. [59], predominantly dominated the AOA community in soil samples without N fertilization (N0 and N0 + S treatments). However, N fertilization yielded the opposite effect on various AOA phylogenetic clades, specifically leading to a relative increase in AOA-Clade B and AOA-Clade Nitrososphaera, and a decrease in AOA-Clade A. AOA-Clade B dominated in soil samples with both low and high fertilizer level (N135, N270, N135 + S, and N270 + S treatments). Alves et al. [60] indicated that AOA-Clade B and AOA-Clade Nitrososphaera exhibited a positive correlation with ammonia concentration compared to AOA-Clade A. Our results further support the notion of the higher ammonia tolerance and growth advantage of AOA-Clade B over AOA-Clade Nitrososphaera. The is not only due to the significantly lower relative abundance of AOA-Clade Nitrososphaera compared to AOA-Clade B, but also because the relative abundance of AOA-Clade Nitrososphaera decreased significantly in plots with high fertilizer levels (N270 and N270 + S treatments), while AOA-Clade B remained relatively stable. Despite the superior adaptability of AOA-Clade B and AOA-Clade Nitrososphaera to ammonia, they exhibited a negative correlation with soil PNR (Figure S4), whereas AOA-Clade A showed a positive and stronger correlation with soil PNR. The trend of AOA-Clade A and AOA-Clade Nitrososphaera observed in this study aligns with the findings of Zhang et al. [42] in acidic soils. In conclusion, AOA-Clade A might significantly contribute to soil potential nitrification more than AOA-Clade B and AOA-Clade Nitrososphaera.
The influence of straw returning on the AOA community was reflected in the change of its α-diversity indices (Table S3). In treatments without straw returning, the N0 treatment showed the highest Chao1 and Shannon indices. However, in treatments with straw applied, these indices notably increased in the N135 + S treatment compared to the N0 + S treatment. This difference indicated that straw returning enhanced the richness and diversity of species under low N fertilization [61]. This was attributed to the unique growth characteristics of AOA-Clade B and AOA-Clade Nitrososphaera, which were stimulated by N fertilization [60], thereby enhancing species growth. Notably, the AOA community of the N135 + S treatment exhibited higher α-diversity due to straw returning but had a lower soil PNR than the N0 + S treatment. One possible explanation for this observation might be that N fertilization reduced the abundance of AOA, resulting in a decrease in the amount of AOA in the soil. In conclusion, our findings suggest that straw returning has a less pronounced effect on the AOA community compared to N fertilization. Additionally, the AOA community’s phylogenetic clade may serve as a better indicator of the nitrification function of AOA.

4.3. Influence of Environmental Factors on AOA Community and Soil Nitrification Dynamics

It appears that the AOA community is affected by environmental factors, particularly nitrogen availability, as indicated by the db-RDA results based on phylogenetic clades (Figure 5). Notably, the soil NH4+/NO3− ratio and N fertilizer application rates were the most important variables shaping the AOA community (Table S4), consistent with findings in a study on rotation of soil with winter wheat and summer maize [62]. PLS-PM analysis further confirmed that the N fertilizer application rates had the highest direct and total effect on the soil PNR (Figure 5; Table S5). Interestingly, the abundance of the AOA amoA gene may not have a direct significant effect. It could influence soil PNR by modulating the AOA community, particularly in its beta diversity (PCoA1; Table S6). This suggests that the composition of AOA, based on phylogenetic clades, has a more substantial direct relationship with soil nitrification function than its abundance alone. However, soil pH emerges as a key factor in predicting soil nitrification, surpassing microbial indices in importance (Table S6). This observation may be due to the fact that soil pH can not only change the community and physiological capabilities of functional microorganisms but also affect their nitrification activity by disrupting the balance between nitrate and ammonia [38,44,63].
Moreover, straw decomposition and related enzyme activities positively impact soil PNR by altering soil properties. However, their influence on soil nitrification appears to be less significant compared to nitrogen fertilization (Figure 5; Table S5). Consequently, the short-term effect of straw on soil nitrification seems limited, necessitating further investigation into its long-term impact.

5. Conclusions

Our study revealed the microbial dynamics of soil nitrification, particularly in response to straw returning and long-term N fertilization. Straw returning mitigated the inhibition of nitrogen fertilization on soil PNR, particularly under low nitrogen fertilization. Long-term N fertilization had a significant negative impact on the abundance of key functional microorganisms like AOA, AOB, and CAOB-cladeB. However, straw application boosted AOA amoA abundance, which correlated with trends in PNR. The shift in AOA community composition from AOA-Clade A towards AOA-Clade B dominance under N fertilization treatment highlighted the microbial response to environmental changes. Furthermore, soil properties played a crucial role in influencing both AOA community composition and soil PNR. The NH4+/NO3− ratio emerged as a particularly influential factor in shaping AOA community composition. Soil pH and the beta diversity of the AOA community were highlighted as pivotal factors influencing soil potential nitrification. Overall, our findings underscore the complex interplay between straw decomposition, N fertilization, soil properties, and AOA community dynamics in regulating soil potential nitrification. Understanding these interactions is essential for effective soil management and the promotion of ecosystem health in agricultural settings.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14071550/s1, Table S1. The primers used for quantitative real-time PCR. Table S2. Effects of fertilization, straw and their interaction on soil chemical and biological characteristics and the amoA gene index. Table S3. Diversity indices of the community composition of ammonia-oxidizing archaea (AOA). Table S4. Soil characteristics correlated with AOA communities based on db-RDA. Table S5. Total, direct, and indirect effects of explanatory variables on soil potential nitrification rate. Table S6. Factor importance on soil potential nitrification rate by Random Forest analysis. Figure S1. Activity of cellulase (A) and xylanase (B) influenced by fertilization and straw. Figure S2. Abundances of AOB (A), CAOB cladeA (B), and CAOB cladeB (C) influenced by fertilization and straw returning. Figure S3. Neighbor-joining phylogenetic tree of ammonia-oxidizing archaea (AOA) amoA gene sequences (representatives with relative abundance >1%). Bootstrap values (>50%) are indicated at branch points. Figure S4. Relationship between soil potential nitrification and sequences of AOA phylogenetic clades.

Author Contributions

Writing–original draft, F.W.; Writing–review and editing, F.W., X.L., and L.L. Formal Analysis, F.W. Investigation, F.W., M.L. and B.G.; Resources, S.L. Methodology, L.L. Supervision, L.L. and J.W. All authors contributed to the article and approved the submitted version. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Basic Scientific Research Project of University in Liaoning [Grant numbers LJKMZ20220995] and the National Natural Science Foundation of China [Grant numbers 42277321].

Data Availability Statement

Data are contained within the article and Supplementary Materials.

Conflicts of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Figure 1. Proportion of maize straw decomposition (A) and rate of soil potential nitrification (B) influenced by fertilization and straw returning. ANOVA P-values are indicated on the graph. F: the effect of nitrogen fertilization; S: the effect of straw returning. F ∗ S: the interaction of nitrogen fertilization and straw returning. Lowercase and uppercase letters represent significant differences between different fertilization treatments in soils without and applied straw, respectively (p < 0.05). N0: control without fertilization. N135: low nitrogen fertilization with 135 kg N hm−2 yr−1 urea chemical fertilizer. N270: high nitrogen fertilization with 270 kg N hm−2 yr−1 urea chemical fertilizer. N0 + S: N0 plus straw. N135 + S: N135 plus straw. N270 + S: N270 plus straw.
Figure 1. Proportion of maize straw decomposition (A) and rate of soil potential nitrification (B) influenced by fertilization and straw returning. ANOVA P-values are indicated on the graph. F: the effect of nitrogen fertilization; S: the effect of straw returning. F ∗ S: the interaction of nitrogen fertilization and straw returning. Lowercase and uppercase letters represent significant differences between different fertilization treatments in soils without and applied straw, respectively (p < 0.05). N0: control without fertilization. N135: low nitrogen fertilization with 135 kg N hm−2 yr−1 urea chemical fertilizer. N270: high nitrogen fertilization with 270 kg N hm−2 yr−1 urea chemical fertilizer. N0 + S: N0 plus straw. N135 + S: N135 plus straw. N270 + S: N270 plus straw.
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Figure 2. Abundances of AOA influenced by fertilization and straw returning. ANOVA p-values are indicated on the graph, and ns indicated no significance. F: the effect of nitrogen fertilization; S: the effect of straw returning. F ∗ S: the interaction of nitrogen fertilization and straw returning. Lowercase and uppercase letters represent significant differences between different fertilization treatments in soils without and applied straw, respectively (p < 0.05). N0: control without fertilization. N0: control without fertilization. N135: low nitrogen fertilization with 135 kg N hm−2 yr−1 urea chemical fertilizer. N270: high nitrogen fertilization with 270 kg N hm−2 yr−1 urea chemical fertilizer. N0 + S: N0 plus straw. N135 + S: N135 plus straw. N270 + S: N270 plus straw.
Figure 2. Abundances of AOA influenced by fertilization and straw returning. ANOVA p-values are indicated on the graph, and ns indicated no significance. F: the effect of nitrogen fertilization; S: the effect of straw returning. F ∗ S: the interaction of nitrogen fertilization and straw returning. Lowercase and uppercase letters represent significant differences between different fertilization treatments in soils without and applied straw, respectively (p < 0.05). N0: control without fertilization. N0: control without fertilization. N135: low nitrogen fertilization with 135 kg N hm−2 yr−1 urea chemical fertilizer. N270: high nitrogen fertilization with 270 kg N hm−2 yr−1 urea chemical fertilizer. N0 + S: N0 plus straw. N135 + S: N135 plus straw. N270 + S: N270 plus straw.
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Figure 3. Relative abundance (A) and principal coordinates analysis (PCoA) (B) of the AOA community. Lowercase and uppercase letters represent significant differences between different fertilization treatments in soils without and applied straw, respectively. N0: control without fertilization. N135: low nitrogen fertilization with 135 kg N hm−2 yr−1 urea chemical fertilizer. N270: high nitrogen fertilization with 270 kg N hm−2 yr−1 urea chemical fertilizer. N0 + S: N0 plus straw. N135 + S: N135 plus straw. N270 + S: N270 plus straw. Ellipses indicate the distribution and separation of data points among different fertilization.
Figure 3. Relative abundance (A) and principal coordinates analysis (PCoA) (B) of the AOA community. Lowercase and uppercase letters represent significant differences between different fertilization treatments in soils without and applied straw, respectively. N0: control without fertilization. N135: low nitrogen fertilization with 135 kg N hm−2 yr−1 urea chemical fertilizer. N270: high nitrogen fertilization with 270 kg N hm−2 yr−1 urea chemical fertilizer. N0 + S: N0 plus straw. N135 + S: N135 plus straw. N270 + S: N270 plus straw. Ellipses indicate the distribution and separation of data points among different fertilization.
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Figure 4. The influence of soil properties on the AOA community based on db-RDA. SOC: soil organic carbon; TN: total nitrogen; NH4+-N: ammonia nitrogen; NO3−-N: nitrate nitrogen; C/N: the ratio of SOC to TN; NH4+-N/NO3−-N: the ratio of ammonia nitrogen to nitrate nitrogen; SR: straw application rates; NR: nitrogen fertilizer application rates; xylanase: the activity of xylanase; cellulase: the activity of cellulase.
Figure 4. The influence of soil properties on the AOA community based on db-RDA. SOC: soil organic carbon; TN: total nitrogen; NH4+-N: ammonia nitrogen; NO3−-N: nitrate nitrogen; C/N: the ratio of SOC to TN; NH4+-N/NO3−-N: the ratio of ammonia nitrogen to nitrate nitrogen; SR: straw application rates; NR: nitrogen fertilizer application rates; xylanase: the activity of xylanase; cellulase: the activity of cellulase.
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Figure 5. The influence of biotic and abiotic factors on soil PNR based on PLS-PM. Red and blue lines indicate positive and negative effects of variable factors, respectively; solid and dotted lines represent the significance and non-significance of the correlation, respectively. The values beside the lines represent the path coefficient. GoF: goodness of fit, representing the fit degree of the model. Straw decomposition includes cellulase and xylanase activity. Soil properties include soil pH, C/N ratio, NH4+/NO3− ratio, and the content of SOC, TN, NH4+, NO3−. AOA amoA community includes PCoA1 of the AOA community and sequences of AOA-Clade A, AOA-Clade B, and AOA-Clade Nitrososphaera.
Figure 5. The influence of biotic and abiotic factors on soil PNR based on PLS-PM. Red and blue lines indicate positive and negative effects of variable factors, respectively; solid and dotted lines represent the significance and non-significance of the correlation, respectively. The values beside the lines represent the path coefficient. GoF: goodness of fit, representing the fit degree of the model. Straw decomposition includes cellulase and xylanase activity. Soil properties include soil pH, C/N ratio, NH4+/NO3− ratio, and the content of SOC, TN, NH4+, NO3−. AOA amoA community includes PCoA1 of the AOA community and sequences of AOA-Clade A, AOA-Clade B, and AOA-Clade Nitrososphaera.
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Table 1. Basic properties of the tested soil before straw returning.
Table 1. Basic properties of the tested soil before straw returning.
SOC
(g kg−1)		TN
(g kg−1)		NH4+-N
(mg kg−1)		NO3−-N
(mg kg−1)		pH
N09.080.743.9727.396.69
N1358.800.702.6317.466.12
N2708.480.7219.4838.164.64
N0: control without fertilization. N135: low nitrogen fertilization with 135 kg N ha−1 yr−1 urea chemical fertilizer. N270: high nitrogen fertilization with 270 kg N ha−1 yr−1 urea chemical fertilizer.
Table 2. Soil properties influenced by fertilization with and without straw returning.
Table 2. Soil properties influenced by fertilization with and without straw returning.
No StrawApplied Straw
N0N135N270N0 + SN135 + SN270 + S
pH6.76 ± 0.02 a6.34 ± 0.03 b4.96 ± 0.02 c7.01 ± 0.04 A6.52 ± 0.01 B6.05 ± 0.06 C
SOC
(g kg−1)		8.71 ± 0.03 a8.44 ± 0.07 c8.66 ± 0.01 b9.52 ± 0.04 A9.22 ± 0.02 B9.02 ± 0.02 C
TN
(g kg−1)		0.75 ± 0.01 c0.78 ± 0.01 b0.86 ± 0.02 a0.76 ± 0.01 C0.88 ± 0.01 B0.97 ± 0.02 A
NH4+-N
(mg kg−1)		9.45 ± 0.25 c10.16 ± 0.06 b11.58 ± 0.23 a13.81 ± 0.14 C14.59 ± 0.09 B20.03 ± 0.51 A
NO3−-N
(mg kg−1)		0.75 ± 0.07 c1.95 ± 0.39 b6.22 ± 0.27 a1.57 ± 0.20 C5.10 ± 0.44 B7.34 ± 0.20 A
SOC: soil organic carbon; TN: total nitrogen; NH4+-N: ammonia nitrogen; NO3−-N: nitrate nitrogen. Lowercase and uppercase letters represent significant differences between different fertilization treatments in soils without and applied straw respectively (p < 0.05). N0: control without fertilization. N135: low nitrogen fertilization with 135 kg N ha−1 yr−1 urea chemical fertilizer. N270: high nitrogen fertilization with 270 kg N ha−1 yr−1 urea chemical fertilizer. N0 + S: N0 plus straw. N135 + S: N135 plus straw. N270 + S: N270 plus straw.
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Wang, F.; Liang, X.; Liang, M.; Guo, B.; Li, S.; Liu, L.; Wang, J. Straw Returning Alleviates the Inhibition of Soil Nitrification Medicated by Ammonia-Oxidizing Archaea under Low Nitrogen Fertilization. Agronomy 2024, 14, 1550. https://doi.org/10.3390/agronomy14071550

AMA Style

Wang F, Liang X, Liang M, Guo B, Li S, Liu L, Wang J. Straw Returning Alleviates the Inhibition of Soil Nitrification Medicated by Ammonia-Oxidizing Archaea under Low Nitrogen Fertilization. Agronomy. 2024; 14(7):1550. https://doi.org/10.3390/agronomy14071550

Chicago/Turabian Style

Wang, Feng, Xiaolong Liang, Minjie Liang, Bingqing Guo, Shuangyi Li, Lingzhi Liu, and Jingkuan Wang. 2024. "Straw Returning Alleviates the Inhibition of Soil Nitrification Medicated by Ammonia-Oxidizing Archaea under Low Nitrogen Fertilization" Agronomy 14, no. 7: 1550. https://doi.org/10.3390/agronomy14071550

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