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Article

Application of Selenocysteine Increased Soil Nitrogen Content, Enzyme Activity, and Microbial Quantity in Camellia oleifera Abel. Forests

by
Jian Li
1,†,
Wei Tang
2,†,
Sheng Lu
1,
Ye Wang
1,
Zuoying Kuang
1 and
Jun Yuan
1,*
1
Forestry College, Central South University of Forestry and Technology, Changsha 410004, China
2
Hunan Academy of Forestry, Changsha 410004, China
*
Author to whom correspondence should be addressed.
†
The author contributed equally to this work.
Forests 2023, 14(5), 982; https://doi.org/10.3390/f14050982
Submission received: 10 March 2023 / Revised: 28 April 2023 / Accepted: 8 May 2023 / Published: 10 May 2023
(This article belongs to the Special Issue Non-timber Forestry Breeding, Cultivation and Processing Technology)
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Abstract

:
The effect mechanism of inorganic selenium on soil fertility has been effectively explained, but the effect of selenocysteine as organic selenium on the soil of Camellia oleifera Abel. forests has not been reported. In this study, the soil of a C. oleifera forests under natural conditions was taken as the control, and four treatments, namely selenocysteine (SeCys), cysteine + sodium selenite (Cys + Se), urea + sodium selenite (Ur + Se), and cysteine (Cys), were set up through a pot experiment to analyze the effects of different treatments on the physicochemical properties and biological characteristics of soil in C. oleifera forests. The results showed that SeCys significantly increased the soil total nitrogen content, nitrate nitrogen, and ammonium nitrogen contents compared with the treatment with inorganic selenium. In addition, the application of SeCys improved the activities of soil urease, soil acid phosphatase, soil nitrate reductase, and soil nitrite reductase on day 24 of culture, while under Cys + Se treatment, the activities of these four enzymes showed significant effects on day 32. The effect of SeCys on increasing the number of soil bacteria and fungi was significantly higher than that of other treatments and increased by 800% and 217%, respectively, compared with the control. SeCys also had significant effects on selenium and nitrogen content of Camellia oleifera seedlings. Correlation analysis showed that soil microbial biomass carbon and nitrogen were significantly correlated with soil enzyme activity, suggesting that SeCys could promote enzyme activity in C. oleifera forests by increasing the microbial number and improving microbial metabolism. The results indicated that SeCys could be used as an ingredient in new high-efficiency fertilizers.

1. Introduction

Selenium (Se) is considered a mineral micronutrient, having unique characteristic physical and chemical properties, which are intermediates of metals and nonmetals [1], and an essential trace element and nutrient element for animals and plants. The accumulation of Se in plants depends on the Se content and bioavailability in the soil [2]. However, the Se content of the soil is low and very widely distributed in the world [3]; therefore, the exogenous application of Se fertilizer to increase the Se content of the soil is an effective method. At present, there are two types of Se in nature: organic and inorganic. The common inorganic Se is mainly elemental Se (Se0), selenide (Se2−), selenite (Se4+), and selenate (Se6+); organic Se is mainly represented by selenocysteine and selenomethionine [4]. In recent years, studies on inorganic Se have been reported in many aspects, such as the effects of Se on crop growth and absorption [5,6], the interaction between Se and metals on plants or soils [7,8,9], and the morphology and transformation of Se in the soil [10]. To date, the application of inorganic Se (selenite and selenate) to the soil as Se fertilizer has become the norm [11]. However, the environmental problems caused by the toxicity and poor effectiveness of Se cannot be ignored [12]. As a type of organic Se, selenocysteine was once used as a type of feed [13]. It has advantages, such as low toxicity and good stability; therefore, it has a good development value in agricultural applications [14,15].
There are insufficient studies on how selenocysteine affects soil biological activity (metabolism, enzyme activity, and microbial biomass). Soil microorganisms and soil enzymes play an important role in the soil and are important indicators for characterizing soil fertility; their participation in organic matter decomposition, nutrient conversion, and nutrient cycling cannot be separated from them [16,17,18,19]. Liu et al. [20] found that selenite would be transformed into a stable and low-toxicity state in the soil, increase persistent free radicals, and thus reduce the abundance and diversity of microorganisms. Yang et al. [7] showed that root application of Se could increase the bacterial abundance in cadmium-contaminated soil and improve the soil microbial community structure. Cheng et al. [21] showed in a pot experiment of rapeseed that Se application could contribute to the enrichment of beneficial rhizosphere microorganisms in rapeseed rhizosphere soil, thus promoting plant growth. This indicates that a change in the Se content of the soil would affect soil microbial quantity and community structure. There has been a serious lack of attention to the effect of Se fertilizer on soil enzyme activity. Tang et al. [22] showed that the effect of exogenous Se on soil biological activity depends on the application level of Se rather than the form of Se, while Shi et al. [23] showed that organic Se was more conducive to the growth of soil microorganisms than inorganic Se and could improve soil enzyme activity. This is paradoxical. Based on previous studies, this study hopes to further elucidate the effects of organic Se represented by selenocysteine on soil enzyme activities. At the same time, whether the application effect of seleno-amino acids is different from that of inorganic Se will be discussed. However, there is a serious lack of attention to whether and how exogenous organic Se affects soil bioactivity. The effects of the application of seleno-amino acid-like selenocysteine as a Se fertilizer on soil bioactivity are worthy of further study.
Camellia oleifera Abel. is one of the four edible woody oil species famous in the world and plays an important role in ensuring national grain and oil security, economic construction, and ecological civilization construction [24]. Characteristics, such as the low fertility of C. oleifera forests and few microorganisms in soil, seriously limit the yield of C. oleifera forests [25]. How to improve the soil fertility of C. oleifera forests has become a research issue of great interest, to which nitrogen and microorganisms have been given more attention [26,27]. Soil nitrogen plays an important role in soil physical, chemical, and biological processes and is the most important nutrient element limiting plant growth [28]. The conversion of nitrogen in the soil is almost entirely driven by microorganisms [29]. Studies have shown that Se not only regulates nitrogen metabolism by affecting soil microbial structure and activity [30,31] but also directly promotes nitrogen absorption by plants [32,33]. At the same time, an increase in nitrogen content reacts with Se to improve the utilization rate of Se by plants [34,35]. It is not clear how effective seleno-amino acid as a Se-amino acid-chelated Se is in these two aspects and whether it differs in promoting nitrogen levels compared with conventional non-chelated Se.
Therefore, it is necessary to study selenocysteine for soil nitrogen content and biological activity in C. oleifera forests. We hypothesized that seleno-amino acids were more effective than non-chelated Se. In this study, selenocysteine was selected as the research material to conduct an indoor pot experiment to explore the effects of selenocysteine on soil microbial characteristics of oil tea camellia forest and further analyze the differences in the effects of selenocysteine and non-chelated selenocysteine on soil nitrogen content, which will lay a scientific basis for the use of selenocysteine as a new fertilizer raw material.

2. Materials and Methods

2.1. Experimental Material Collection and Design

2.1.1. Experimental Materials

The experimental soil was collected from the C. oleifera forest (28°30′ N, 122°50′ E), Dongcheng Town, Wangcheng District, Changsha City, Hunan Province, China. The altitude is 50 m; the terrain is hilly; the planted tree is C. oleifera ‘Huajin’; the age of the tree is 9 years; and the plant row spacing is 2 m × 3 m. The soil type in this region is red soil with heavy viscosity, a soil bulk density of 0.086 g/cm3, and a water content of 16.14%. It is a subtropical monsoon humid climate, with four distinct seasons: a hot summer, rainy summer, mild winter, and humid winter. The average annual temperature is 16.8–17.2 °C, and the annual precipitation is 1422.4 mm.

2.1.2. Experimental Design and Treatments

A pot experiment was used in this study. In a 1-hectare C. oleifera forest, 20 C. oleifera trees with similar growth and evenly divided in the forest were selected. After removing the surface floating soil and litter, 100 g soil was collected from 0–20 cm soil layer of each C. oleifera using S-type sampling method, and the collected soil was mixed. After returning to the laboratory, the collected soil samples were immediately placed in a clean indoor ventilated area and spread out to air dry naturally. The air-dried soil samples were sieved through a 2 mm screen and stored in plastic bags in batches at 24 °C, then used for cultivation. The bare root seedlings of the annual ‘Huajin’ C. oleifera were taken (planting depth of about 7 cm) and planted in a pot with 250 g of sifted soil. The seedlings were placed in a greenhouse for 1 month. Four treatment groups were designed in this study: selenocysteine (SeCys), cysteine + sodium selenite (Cys + Se), urea + sodium selenite (Ur + Se), and cysteine (Cys). These treatments were set up to explore the role of the amino acid selenium, keeping nitrogen and selenium levels constant. According to the preset soil selenium concentration of 8 mg/kg, 0.0922 g of selenocysteine was weighed for SeCys; 0.0614 g of cysteine and 0.0876 g of sodium selenite were weighed for Cys + Se; 0.0152 g of urea and 0.0876 g of sodium selenite were weighed for Ur + Se; and 0.0614 g of cysteine was weighed for Cys. Each treatment was configured as a 1 L solution. Meanwhile, pure water was used as a control (CK) in this experiment. Then, 50 mL of solution was applied to each cup of seedlings according to its group (reagent source: urea, cysteine, and selenocysteine were produced by Sinopsin Chemical Reagent Co. Ltd. (Changsha, China), and the sodium selenite was produced by Chengdu Borite Chemical Technology Co. Ltd. (Chengdu, China)). All reagents were analytically pure. The final substrate concentration in the soil of the four treatment groups was SeCys (17.03 mg/kg), Se (17.52 mg/kg) + Cys (12.29 mg/kg), Se (17.52 mg/kg) + Ur (6.09 mg/kg), Cys (12.29 mg/kg). Each treatment was repeated 15 times, and a random block design was performed. Samples were taken on days 3, 6, 12, 24, and 32 of the experiment. Each time, three samples were randomly selected from each treatment and brought back to the laboratory to separate C. oleifera seedlings and soil. C. oleifera seedlings were dried, weighed, and crushed by a ball mill and screened at 0.15 mm for the determination of selenium and nitrogen content. The soil was screened at 2 mm, and the physical, chemical, and biological properties of the soil were determined. In addition, these times were defined by us as short time (days 3, 6, 12) as well as long time (days 24, 32) in terms of the changes in soil properties we observed. Short time indicated that the time of activating enzyme activity was shorter. The longer the time point was, the longer the activation time was.

2.2. Test Methods

2.2.1. Determination of the Physical and Chemical Properties of Soil

Soil pH was determined using a pH meter in a 1 mol/L potassium chloride suspension with a soil/liquid ratio of 1:2.5 [36]. The soil bulk density was measured using the ring knife method, and the water content was measured using the drying process method [37]. The total selenium content of soil was determined by atomic fluorescence spectrometry, and 2 g of soil sample was weighed and placed in a 100 mL triangle bottle; 10 mL of mixed acid (volume ratio 3:2) of HNO3 and HClO4 was added, and then it was nitrated in an automatic temperature controlled nitrification furnace until white smoke was emitted. After that, 10 mL HCl (6 mol/L) was added and heated in boiling water bath for 10 min. After cooling, the volume was fixed with deionized water, and the selenium content was determined after mixing evenly [38]. The total nitrogen of the soil was determined using the H2SO4–H2O2 method combined with boiling and automatic chemical analyzer determination (Smartchem200, West Co Scientific Instruments, Rome, Italy). Soil nitrate nitrogen and ammonium nitrogen were determined using 1 mol/L KCI solution and the automatic chemical analyzer (Smartchem200, West Co Scientific Instruments, Rome, Italy) [39].

2.2.2. Soil Enzyme Activity Determination

Air–dried soil passed through a 1 mm sieve was used to measure soil enzyme activity. The culture systems of soil urease and acid phosphatase (S-ACP) were operated by adding 10 mL urea (10 g/mL) and 5 mL disodium phenyl phosphate (0.5 g/mL) substrates to the soil and then incubated at 37 °C for 24 h. The culture systems of soil nitrate reductase (S-NR) and nitrite reductase (S-NIR) were operated by researchers adding 1 mL potassium nitrate (0.01 mg/mL) and 1 mL sodium nitrite (0.5 g/mL) substrates to the soil and then incubated at 37 °C for 24 h. Urease, S-NR, S-NIR, and acidic S-ACP activities were expressed as mol urea s−1, mol nitrate s−1, mol nitrite s−1, and mol phenol s−1, respectively. The UV spectrophotometer, UV-2600, Shimadzu, Japan, was used for spectrophotometric measurements at the wavelengths of 578 nm (urease), 570 nm (acid S-ACP), and 520 nm (S-NR, S-NIR) [40,41].

2.2.3. Measurement of Soil Microbial Quantity

The number of microorganisms was determined using the dilution-coated plate method [42]. The culture dish was a disposable plastic culture dish, the bacterial medium was nutrient broth (Solarbio) agar (BioFroxx) medium, and the fungal medium was Bengal red (Solarbio) agar (BioFroxx) medium. Before inoculation, soil microbes were extracted from soil using sterile water. In detail, 10−1 soil diluent was prepared by shaking 10 g soil and 90 mL sterile water together on a thermostat oscillator at 200 r/min for 20 min followed by a 5 min standing. Then, different gradient diluents were prepared by diluting the 10−1 soil diluent using sterile water and then using inoculation. The inoculation was carried out on a sterile operating table, and the plate was incubated in an inverted incubator. The bacteria were incubated at 37 °C for 3 days, and the fungi were incubated at 28 °C for 3 days. If the number of colonies in the three plates with the same dilution was similar, then the colony-forming unit was calculated and the average was determined. If one plate was very different from the other two, the average of the two small differences was taken, or the plate was coated again. Finally, the average number of colonies with different dilutions was determined.

2.2.4. Determination of Soil Microbial Biomass Carbon and Nitrogen

The soil microbial biomass carbon and nitrogen were fumigated using chloroform; the soil was extracted with 0.5 mol/L K2SO4 solution, and the filtrate obtained after filtration was measured using the total organic carbon instrument (TOC-Vcph, Shimadzu corporation, Shimadzu, Japan) [43].

2.2.5. Determination of Selenium and Nitrogen Content in C. oleifera Seedlings

Plant selenium was measured by hydride atomic fluorescence spectrometry, and 0.2 g of C. oleifera seedlings sample was weighed and placed in a digestion tube; 10 mL HNO and 2 mL H2O2 were added for digestion in a microwave digester. After that, it was heated on an electric heating plate until dry, and 5 mL HCl (6 mol/L) was added until the white smoke was produced. After cooling, it was transferred to a 10 mL volumetric flask, and 2.5 mL potassium ferricyanide solution (100 g/L) was added. The volume was fixed with deionized water, and the selenium content was determined after mixing evenly [44]. The nitrogen of C. oleifera seedlings was determined using the H2SO4–H2O2 method combined with boiling and nitrogen analyzer determination [45].

2.3. Data Analysis

SPSS 22.0 software was used for the analysis of variance and linear regression analysis of the experimental data, and Duncan’s test was used for multiple comparisons. Different lowercase letters indicate the significant difference of each reagent treatment at p < 0.05, and the data in the table are presented as mean ± standard deviation. The charts were drawn using Microsoft Excel 2020 and SPSS 22.0 software. The heat map was drawn using the Lingbo microlesson.

3. Results and Analysis

3.1. Soil pH

The effects of different treatments on the soil pH of C. oleifera forest were significant on days 3 and 32 (Figure 1). During the whole culture period, the trend of all treatments was not obvious. Cys (4.51) increased significantly on day 32 of culture compared with CK but was close to the control level at other times. Meanwhile, there was no significant difference in SeCys and Ur + Se compared with the control.

3.2. Soil Total Selenium

The variation trend of SeCys was first increased and then decreased, and it reached the maximum on day 24 (5.54 mg/kg) (Figure 2). Cys + Se showed an opposite trend to that of Ur + Se after day 24. Cys had a significant effect on the total selenium content of soil during the whole culture period and reached the maximum value on day 3 (5.65 mg/kg). Ur + Se significantly increased total selenium on days 6 and 32.

3.3. Soil Nitrogen

The effects of different treatments on soil nitrogen content are different (Figure 3). During the whole culture period, the trend of total nitrogen content under SeCys treatment was similar to that under CK treatment and decreased after reaching the maximum on day 24, while Cys + Se and Ur + Se showed approximately opposite trends. Compared with CK treatment, both significantly increased soil total nitrogen content within 6 days of culture (p < 0.05), but SeCys still showed a significant difference on day 12, which was 3% higher than CK treatment. Cys significantly increased soil total nitrogen content on day 32 (p < 0.05) by 43% higher than CK treatment. SeCys significantly increased (p < 0.05) the nitrate nitrogen and ammonium nitrogen contents of the soil on day 3 of culture by 25% and 44%, respectively, compared with CK. Subsequently, the performance was insignificant and even had negative effects on day 12; however, soil ammonium nitrogen content increased significantly on day 32 (p < 0.05). Cys + Se and Ur + Se showed no significant effect on soil nitrate nitrogen content, but Ur + Se significantly increased (p < 0.05) soil ammonium nitrogen content throughout the culture period compared with the control and reached the maximum of 81% higher than CK treatment on day 24. Cys significantly increased soil nitrate nitrogen content on days 3 and 24 of culture and showed no significant effect on soil ammonium nitrogen content after day 3.

3.4. Soil Enzyme Activity

The effects of different treatment groups on soil enzyme activities are also significantly different. For soil urease, Cys + Se and Cys showed an increasing trend, while SeCys and Ur + Se showed no significant change (Figure 4A). Compared with the control, SeCys significantly increased the soil urease activity on days 6 and 24 (p < 0.05) by 119% and 37%, respectively, and reached the maximum on day 6, but SeCys showed a negative effect on day 12. Compared with CK, Cys significantly increased the soil urease activity from 2.30% to 43% during the whole culture period (p < 0.05) and reached the maximum on day 12. Urease activity maintained a stable increasing trend under Cys + Se treatment and reached the maximum value on day 32; it increased significantly by 54% compared with CK treatment (p < 0.05). Ur + Se treatment showed no effects during the whole culture period compared with other treatment groups. For S-NR (Figure 4B) and S-NIR (Figure 4C), the trend of SeCys treatment was similar to that of CK treatment; it decreased within 12 days and showed significantly negative effects on day 12, then increased and decreased, and then increased significantly (p < 0.05) on day 24 by 68% and 33%, respectively, compared with CK treatment. The treatment with Cys showed an increasing trend within 6 days and then decreasing, and both significantly increased soil NR and NIR activity compared with CK on day 6 by 82% and 118%, respectively (p < 0.05), and it also showed a significant effect on soil NR activity on day 12 (p < 0.05). The trend of S-NR and S-NIR in the case of Cys + Se was opposite to that of SeCys and reached the maximum value on day 32, increased by 105% and 51%, respectively, compared with CK. The trend of Ur + Se in the whole culture period was not obvious on S-NR and S-NIR. Compared with the control, Ur + Se had a negative effect on day 24 and significantly increased S-NR activity from 23% to 87% at other times (p < 0.05), reaching the maximum on day 3. Ur + Se significantly increased S-NIR activity from 7% to 45% after day 6 (p < 0.05) and reached the maximum on day 12. For S-ACP, the trend of Cys + Se and Cys first increased and then decreased, while SeCys and Ur + Se showed the same trend as S-NR and S-NIR (Figure 4D). The S-ACP activity of SeCys increased significantly on day 24 (p < 0.05) by 70% higher than that of CK. The S-ACP activity of Cys increased significantly on days 6 and 12 (p < 0.05) by 92% and 55%, respectively, compared with that of CK. Cys + Se reached the maximum value on day 32, increasing by 54%. Ur + Se was similar to Cys + Se and significantly increased by 68% on day 32 compared with CK; both showed a significant effect on day 12.

3.5. Soil Fungi and Bacteria Numbers

SeCys showed a significant effect on soil microbial number in C. oleifera forest (Figure 5). During the whole culture period, the overall trend of different treatment groups was first increasing and then decreasing. The number of bacteria and fungi under SeCys treatment significantly increased on days 6 and 12 (p < 0.05), and both reached the peak on day 6, increasing by 800% and 217%, respectively, compared with that of CK treatment. Cys + Se treatment showed a significant effect on the number of fungi on day 32 of culture compared with CK (p < 0.05). Although there were significant effects on fungi on day 6 and 24, as well as on bacteria on day 24 and 32, they were lower than SeCys. The trend of the effect of Ur + Se treatment on the number of fungi was similar to that of Cys + Se treatment on the number of fungi, and the number of fungi in the soil of C. oleifera forest increased significantly on day 3 of culture (p < 0.05) compared with treatment with CK; the number of bacteria was insignificant. Cys significantly increased the number of soil bacteria after day 3 compared with CK (p < 0.05), and the number of fungi showed no significant effect on day 24 and significantly increased at other times (p < 0.05), compared with CK.

3.6. Soil Microbial Biomass Carbon and Nitrogen Contents

The soil microbial biomass carbon (MBC) and microbial biomass nitrogen (MBN) contents in different treatment groups showed significant differences in different culture periods (Figure 6). During the whole culture period, the trend of MBC and MBN in the case of SeCys was first increasing and then decreasing. On day 24, the MBC and MBN contents reached a peak and showed significant effects compared with other treatment groups (p < 0.05); both increased by 63% compared with CK treatment. The trend of MBN under Cys + Se treatment was similar to that under SeCys treatment, but the trend of MBC was the opposite. Compared with other treatment groups, the MBC and MBN contents increased significantly on day 32 of culture (p < 0.05) by 36% and 129%, respectively, compared with CK treatment. The trends of MBC and MBN contents of Ur + Se and Cys were similar. The trend of MBC was decreasing and then increasing, and the trend of MBN was similar to CK. Compared with the control, Ur + Se significantly increased the content of MBC from −2% (day 24) to 77% (day 6) during the whole culture period and reached the maximum on day 3 (p < 0.05). It also significantly increased the content of MBN from 6% (day 24) to 45% (day 6) during whole culture period and reached the maximum on day 12 (p < 0.05). Cys significantly increased the content of MBC from −8% (day 24) to 112% (day 6) during the whole culture period, compared with the control, and reached the maximum on day 3 (p < 0.05). It also significantly increased the content of MBN from 3% (day 32) to 69% (day 3) during the whole culture period and reached the maximum on day 12 (p < 0.05).

3.7. Selenium and Nitrogen Contents of C. oleifera Seedlings

The selenium content of C. camellia seedlings absorbed by different treatments had great difference (Figure 7A). During the whole culture period, the trend of SeCys was first decreasing and then increasing. SeCys increased significantly on day 3 (0.67 mg/kg), day 12 (0.78 mg/kg), and day 32 (0.58 mg/kg) of culture compared with CK (p < 0.05). The trend of Cys + Se was opposite to that of SeCys, which reached the maximum value (0.63 mg/kg) on day 24 and also had a significant effect on day 6 (p < 0.05). The overall trend of Ur + Se was first increased and then decreased, which had a significant effect on day 6 compared with CK (p < 0.05).
The variation amplitude of different treatments on C. oleifera seedlings nitrogen content are different (Figure 7B). Among all treatments, compared with CK, SeCys significantly increased C. oleifera seedlings nitrogen from 3% (day 3) to 22% (day 32) during the whole culture period (p < 0.05); Cys + Se significantly increased C. oleifera seedlings nitrogen from 3% (day 3) to 12% (day 32) during the whole culture period (p < 0.05); Ur + Se significantly increased C. oleifera seedlings nitrogen from 4% (day 3) to 11% (day 12) during the whole culture period (p < 0.05); Cys significantly increased C. oleifera seedlings nitrogen from 2% (day 3) to 12% (day 12) during the whole culture period (p < 0.05).

3.8. Correlation Analysis

As shown in Figure 8, the number of bacteria and fungi under different treatments was not significantly correlated with soil pH and total nitrogen. The number of bacteria was negatively correlated with the ammonium nitrogen content (p < 0.01, r = −0.347). The number of fungi was negatively correlated with nitrate nitrogen (p < 0.01, r = −0.309) and showed a significant negative correlation with ammonium nitrogen (p < 0.001, r = −0.402). The number of bacteria was not significantly correlated with soil enzyme activity, while the number of fungi was significantly positively correlated with soil urease activity (p < 0.05, r = 0.247) but was not significantly correlated with the other three enzymes. At the same time, there was no significant correlation between the number of bacteria and fungi and MBC and MBN. There was a significant negative correlation between MBC and nitrate nitrogen (p < 0.05, r = −0.271). However, MBC was significantly positively correlated with soil urease, S-NR, and S-ACP activities (p < 0.001, r = 0.565, r = 0.512, and r = 0.511) and showed a significant positive correlation with S-NIR (p < 0.01, r = 0.350). MBN showed a significant positive correlation with soil urease and S-NIR (p < 0.05, r = 0.282, and r = 0.291). It was significantly positively correlated with S-NR activity (p < 0.001, r = 0.442) and S-ACP activity (p < 0.01, r = 0.333). In addition, nitrate nitrogen showed a significant negative correlation with S-NR (p < 0.01, r = −0.323) and a significant negative correlation with S-NIR (p < 0.05, r = −0.258). Ammonium nitrogen had a significant negative correlation with soil urease activity (p < 0.05, r = −0.250). Soil total selenium was significantly positively correlated with selenium in C. oleifera (p < 0.001, r = 0.969); significantly positively correlated with the contents of fungi, ammonium nitrogen, and C. oleifera nitrogen (p < 0.05, r = 0.293, r = 0.253, and r= 0.237); and significantly negatively correlated with nitrate nitrogen (p < 0.001, r = −0.666). The Se content of C. oleifera was significantly positively correlated with soil fungi (p < 0.01, r = 0.326), negatively correlated with soil nitrate nitrogen (p < 0.001, r = −0.640), and positively correlated with soil ammonium nitrogen (p < 0.05, r = 0.294). The nitrogen content of C. oleifera was positively correlated with soil total nitrogen (p < 0.001, r = 0.539).

4. Discussion

4.1. Effects of Selenocysteine on Soil Nutrients of C. oleifera Forest

The direct effects of selenocysteine and other treatment groups may be the reason for the difference in soil total nitrogen content [46], while the indirect effect of the number of soil microorganisms mediated by selenocysteine and other treatment groups may be the reason for the difference in available nitrogen [47]. This study shows that all treatment groups improved the soil total nitrogen content to some extent because all treatments are applied to the soil as a source of nitrogen [48]. On the one hand, selenocysteine kept the soil total nitrogen content at a high and stable level within 12 days, which may be closely related to the promotion of soil microbial activity [49], while the cysteine + sodium selenite treatment did not have significant or even negative effects after day 6.In due course, sodium selenite, possibly because it was applied to the soil as a Se fertilizer and could directly interact with the roots of C. oleifera, was conducive to the absorption of soil nitrogen by C. oleifera [50,51]. On the other hand, selenocysteine significantly increased the ammonium nitrogen content of the soil on days 3 and 32 but did not have significant or even negative effects from day 6 to day 24. It also had a certain effect on the nitrate nitrogen content of the soil. This may be because selenocysteine is decomposed, and the release of selenium increases the absorption of p-available nitrogen, which is consistent with the effect of cysteine + sodium selenite. Urea is a rapidly available ammonium nitrogen fertilizer [52]. However, selenocysteine has a more significant effect than urea + sodium selenite on day 3, suggesting that selenocysteine may also have the same properties as urea, but the specific mechanism is still unclear. Cysteine treatment has the best effect on soil nitrate nitrogen content, followed by selenocysteine. This indicates that the stability of selenocysteine was better than that of cysteine. In other words, the decomposition of selenocysteine produced a large amount of ammonium nitrogen, and it took time for selenocysteine to be converted into nitrate nitrogen. In fact, ammonium nitrogen treated with selenocysteine showed a downward trend before day 12, which may be because ammonium nitrogen was mainly absorbed by C. oleifera seedlings with selenocysteine treatment before day 12. Regarding the increasing trend of ammonium nitrogen content in the later period, it may be related to the increase in microbial quantity promoted by selenocysteine in this study and the enhancement of soil enzyme activity. The correlation showed that available nitrogen content was significantly negatively correlated with the number of microorganisms and biomass. In pot cultivation, soil moisture and nutrients are limited to microorganisms due to plant growth. Studies have shown that nitrogen fertilizers may exacerbate water restriction by promoting plant growth, which in turn reduces the availability of soil microbial substrates and limits microbial growth and population size [53,54]. However, total nitrogen and pH were not significantly correlated with the number of microorganisms and biomass, which might be due to microbial changes having little effect on soil total nitrogen and pH [55]. In conclusion, selenocysteine is more effective than cysteine + sodium selenite in increasing soil nitrogen content.

4.2. Effects of Selenocysteine on Soil Enzymes in C. oleifera Forest

There were significant differences in soil enzyme activities (urease, S-ACP, S-NR, and S-NIR) under different treatments, which were reflected in the time of enzyme activation. Cysteine achieved a significant effect on soil urease activity in a short time, followed by selenocysteine; cysteine + sodium selenite used the longest time. We have already known that the increase in selenium in soil is conducive to the absorption of nitrogen by C. oleifera seedlings, so organic matter in the cysteine + sodium selenite treatment was first absorbed by C. oleifera seedlings. The reason why the soil urease activity increased significantly after a long time by cysteine + sodium selenite treatment is that selenium can also promote the growth of microorganisms and promote the secretion of enzymes. The activity of soil acid phosphatase was similar to that of urease. The activation time of soil nitrate reductase and soil nitrite reductase by urea + sodium selenite was the shortest, followed by cysteine and selenocysteine; cysteine + sodium selenite was the longest. As a small molecular nitrogen source, cysteine can be directly and rapidly absorbed by soil microorganisms [56], thus increasing soil enzyme activity. Urea is a nitrogen compound, and the application of urea to the soil can promote soil nitrate reductase and nitrite reductase, which is consistent with the results of available nitrogen in this study. Selenocysteine significantly activated soil urease activity on days 6 and 12, which was consistent with the results of the effect of selenomethionine on soil urease reported by Shi et al. [23,57]. The effects of selenocysteine and cysteine + sodium selenite on urease activity were different, which may be due to the difference in the adsorption of different forms of Se in the soil [58], resulting in the difference in the number of microorganisms. Studies have shown that the stability of ionic bonds formed by combining different levels of selenium with hydroxides, iron oxides, and organic matter in soil is different, and this stability is also related to soil chemical properties [59,60]. Selenocysteine was stronger on the activation of nitrate reductase and nitrite reductase in the soil than cysteine + sodium selenite. This effect is reflected in the short activation time of the enzyme, which may be because selenocysteine can be absorbed and used by soil microorganisms more quickly. This also explains why selenocysteine has a more significant effect on the promotion of available nitrogen content than cysteine + sodium selenite in this study. The effects of different treatments on the activity of soil acid phosphatase were consistent with those of soil urease. Nowak et al. [61] found that when the application level of exogenous Se was between 3.95 and 39.5 mg/kg, it had no significant effect on soil phosphatase activity. This is inconsistent with the results of this study, which may be because this experiment did not apply sodium selenite alone, and the addition of organic matter can also affect the change in soil enzyme activity [62]. In addition, it may be related to the nitrogen and phosphorus balance in the soil. The increase in nitrogen content in the soil stimulates the secretion of a large number of enzymes that decompose organic nitrogen. Under the condition of adequate nitrogen supply, the demand for phosphorus is also increased, and the microorganisms secrete a large amount of phosphatase to obtain phosphorus from the soil [22]. It has also been shown that nitrogen mineralization can inhibit the synthesis of new enzymes [63], which seems to be inconsistent with the increase in phosphatase. That’s probably because the C. oleifera seedlings can absorb available nitrogen, reducing or inhibiting this effect. The correlation analysis shows that there is a significant negative correlation between available nitrogen and nitrogen-related soil enzyme activity, which is inconsistent with the results of the nitrogen application experiment conducted by Zhang et al. [64] in the spruce forest soil of Tianshan Mountain using the nitrogen deposition gradient method. It may be that in addition to nitrogen, Se was added in this experiment, which improved the absorption of available nitrogen by microorganisms and increased the number of microorganisms in the soil.

4.3. Effects of Selenocysteine on Soil Microbial Characteristics of C. oleifera Forest

At present, the effects of exogenous Se on soil microorganisms are not well understood. In this study, it was found that the application of selenocysteine significantly increased the number of soil microorganisms (bacteria and fungi) in C. oleifera forest compared with other treatment groups, which may be due to the direct utilization of selenocysteine by microorganisms. Some studies have shown that selenocysteine can be used as raw materials in protein synthesis by microorganisms [65], but its absorption mechanism needs to be further studied. Compared with the control group, cysteine + sodium selenite significantly increased the number of bacteria and fungi in the soil of C. oleifera forest, but the effect was not obvious compared with selenocysteine. On the one hand, sodium selenite could be adsorbed and fixed by the sesquioxide and clay minerals in the soil [66]. Li et al. [67] found that selenite absorption may share a common pathway with phosphate absorption, and plant roots could directly absorb selenite [68]. On the other hand, some studies have shown that the volatilization of Se in the soil is partly due to its properties, and the other part is because the chemical morphology of Se changes after it is absorbed by soil microorganisms and plants, and it is volatilized out of the soil [69]. It has also been found that cells are more likely to absorb selenium from organic selenium through endocytosis than inorganic selenium, but the transport and absorption of selenocysteine by microorganisms and plants needs further study [70]. Selenocysteine is a chelated Se fertilizer, in which Se is protected from environmental factors, such as pH value, lipids, fibers, oxalates, oxides, phytic acids, phosphates, and mycotoxins, so it can be effectively absorbed [71]. In addition, urea + sodium selenite showed a rapid effect, which increased faster than the effect in other treatment groups in the early stage of culture, while cysteine + sodium selenite showed a slow effect on the number of fungi; even after a long period of culture, the effect was better, which confirmed the change in soil enzyme activity in this study.
MBC and MBN are important mediators for nutrient conversion, carbon and nitrogen fixation, and mineralization of soil organic matter, as well as important sources and sinks of soil nutrient flow and the carbon and nitrogen cycles [72,73]. Urea + sodium selenite and cysteine significantly increased the carbon and nitrogen content of microbial biomass for a short period of culture, while cysteine + sodium selenite showed a significant effect on day 32 of culture, indicating that urea + sodium selenite and cysteine had a rapid effect, while cysteine showed a slow effect. This is consistent with the conclusions on soil enzyme activity and microbial population (bacteria and fungi) in this study. Selenocysteine has a good effect on the carbon and nitrogen contents of microbial biomass after a long time of culture, which is inconsistent with the peak value of the microbial quantity in this study and may be caused by the death of some microorganisms in the culture process, accumulation in the soil, and decomposition and utilization by other microorganisms in the later stage. MBC and MBN were significantly correlated with available nitrogen content and soil enzyme activity, indicating that MBC and MBN were significantly positively correlated with soil enzyme activity. We all know that soil microorganisms are important sources of soil enzymes [74]. However, selenocysteine significantly increased the number of soil bacteria and fungi. Therefore, we believe that selenocysteine can promote soil nitrogen content and enzyme activity in C. oleifera forest by regulating microbial metabolism.
In conclusion, selenocysteine can significantly promote the number of soil microorganisms, and the soil microbial activity is still active for a long time. We believe selenocysteine has good fertilizer conservation properties.

4.4. Effects of Selenocysteine on Selenium and Nitrogen Content of Plants and Soils

Selenocysteine had a significant effect on selenium and nitrogen contents of Camellia oleifera. It was found in this study that selenocysteine could rapidly increase the selenium content of C. oleifera seedlings in a short time compared with other treatments, indicating that selenocysteine could be used by plants more quickly. This is consistent with the partial correspondence of microorganism above. Selenocysteine also had a significant effect on the 12th day, possibly because during this period, microorganisms became active and nitrogen content in soil increased, which accelerated the absorption of selenium by plants [34]. Similar results were found for cysteine + sodium selenite and urea + sodium selenite. In addition, we found that the nitrogen content of C. oleifera treated with selenocysteine increased the most from day 6 to day 12, and the soil microbial population of C. oleifera forest treated with selenocysteine increased significantly during these two periods. At the same time, the soil total selenium content of selenocysteine increased significantly on day 24, which was consistent with the significant increase time of soil nitrogen-related enzyme activity caused by selenocysteine in this study. It showed that selenocysteine may increase soil nitrogen content by promoting microbial and enzyme activity and further promote the nitrogen content of C. oleifera. There was a significant positive correlation between soil total selenium and C. oleifera selenium, which indicated that applying selenium in soil was beneficial to the enrichment of selenium in C. oleifera. The selenium content of C. oleifera was positively correlated with the number of soil fungi, indicating that selenocysteine promoted the selenium absorption of C. oleifera by regulating the number of microorganisms. However, there was a significant negative correlation between selenium content and nitrate nitrogen in soil, which may be attributed to the increase in microbial activity in soil, which promoted the absorption of nitrate nitrogen in C. oleifera. The nitrogen content of C. oleifera was significantly positively correlated with soil total nitrogen and total selenium, which further confirmed our conclusion.

5. Conclusions

In this study, the overall trend of nitrate nitrogen and ammonium nitrogen contents, S-NR, S-NIR, and S-ACP in the case of SeCys was first decreasing and then increasing, while the trend of soil total Se, total nitrogen, fungi and bacterial quantity, and MBN was first increasing and then decreasing. Additionally, the trend of soil pH, soil urease, and MBC in the whole period was not obvious. Compared with the treatment with inorganic Se, SeCys supplementation significantly increased the total nitrogen content of the soil and had more obvious effects on nitrate nitrogen and ammonium nitrogen contents. In addition, the activation time of nitrogen-related soil enzymes was shorter under SeCys treatment than under Cys + Se treatment. The effect of SeCys on increasing the number of soil bacteria and fungi was significantly more pronounced than that of other treatment groups. In addition, SeCys increased by 800% and 217%, respectively, compared with the control group. SeCys also had significant effects on selenium and nitrogen content of Camellia oleifera. Soil microbial biomass carbon and nitrogen were significantly correlated with soil enzyme activity, suggesting that SeCys could promote and enzyme activity in C. oleifera forest by regulating microbial metabolism. The correlation of selenium and nitrogen contents in C. oleifera with soil microorganisms and nitrogen contents showed that SeCys could promote the selenium and nitrogen absorption of C. oleifera by regulating the number of microorganisms and the activity of soil enzyme. The results indicate that SeCys could be used as an ingredient of new high-efficiency fertilizers.

Author Contributions

Conceptualization, J.Y.; methodology, J.L.; software, J.L., Y.W. and Z.K.; writing—original draft preparation, J.L.; writing—review and editing, J.L., J.Y., W.T., Y.W. and S.L.; visualization, J.L.; supervision, J.Y. and J.L.; project administration, J.Y. and J.L.; funding acquisition, J.Y. and W.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Natural Science Foundation of Hunan Province of China (2021JJ31155) and the Forestry Technology Extension of Hunan, China (grant number [2022]XT24).

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict to interest.

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Figure 1. Effects of different treatments on soil pH value in Camellia oleifera forest. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
Figure 1. Effects of different treatments on soil pH value in Camellia oleifera forest. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
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Figure 2. Effects of different treatments on soil total selenium in Camellia oleifera forest. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
Figure 2. Effects of different treatments on soil total selenium in Camellia oleifera forest. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
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Figure 3. Effects of different treatments on soil nitrogen content of Camellia oleifera forest. (A) Soil total nitrogen contents, (B) Soil nitrate nitrogen contents, (C) Soil ammonium nitrogen contents. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
Figure 3. Effects of different treatments on soil nitrogen content of Camellia oleifera forest. (A) Soil total nitrogen contents, (B) Soil nitrate nitrogen contents, (C) Soil ammonium nitrogen contents. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
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Figure 4. Effects of different treatments on soil enzyme activities in Camellia oleifera forest. (A) Soil urease activity, (B) S-NR activity, (C) S-NIR activity, (D) S-ACP activity. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
Figure 4. Effects of different treatments on soil enzyme activities in Camellia oleifera forest. (A) Soil urease activity, (B) S-NR activity, (C) S-NIR activity, (D) S-ACP activity. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
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Figure 5. Effects of different treatments on soil fungal and bacterial numbers in Camellia oleifera forest. (A) Soil fungi quantity, (B) Soil bacterial quantity. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
Figure 5. Effects of different treatments on soil fungal and bacterial numbers in Camellia oleifera forest. (A) Soil fungi quantity, (B) Soil bacterial quantity. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
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Figure 6. Effects of different treatments on soil microbial biomass C and N contents in Camellia oleifera forest. (A) Soil MBC contents, (B) Soil MBN contents. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
Figure 6. Effects of different treatments on soil microbial biomass C and N contents in Camellia oleifera forest. (A) Soil MBC contents, (B) Soil MBN contents. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
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Figure 7. Effects of different treatments on selenium and nitrogen contents in Camellia oleifera seedlings. (A) Se contents, (B) Nitrogen contents. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
Figure 7. Effects of different treatments on selenium and nitrogen contents in Camellia oleifera seedlings. (A) Se contents, (B) Nitrogen contents. Note: the lowercase letters indicate a significant difference of 0.05 level between different treatments at the same time, and the uppercase letters indicate a significant difference of 0.05 level at different times under the same treatment.
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Figure 8. Correlation analysis of microbial indexes with soil property and Camellia oleifera indexes. Note: * indicates p < 0.05, ** indicates p < 0.01, and *** indicates p < 0.001; r represents the correlation coefficient.
Figure 8. Correlation analysis of microbial indexes with soil property and Camellia oleifera indexes. Note: * indicates p < 0.05, ** indicates p < 0.01, and *** indicates p < 0.001; r represents the correlation coefficient.
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MDPI and ACS Style

Li, J.; Tang, W.; Lu, S.; Wang, Y.; Kuang, Z.; Yuan, J. Application of Selenocysteine Increased Soil Nitrogen Content, Enzyme Activity, and Microbial Quantity in Camellia oleifera Abel. Forests. Forests 2023, 14, 982. https://doi.org/10.3390/f14050982

AMA Style

Li J, Tang W, Lu S, Wang Y, Kuang Z, Yuan J. Application of Selenocysteine Increased Soil Nitrogen Content, Enzyme Activity, and Microbial Quantity in Camellia oleifera Abel. Forests. Forests. 2023; 14(5):982. https://doi.org/10.3390/f14050982

Chicago/Turabian Style

Li, Jian, Wei Tang, Sheng Lu, Ye Wang, Zuoying Kuang, and Jun Yuan. 2023. "Application of Selenocysteine Increased Soil Nitrogen Content, Enzyme Activity, and Microbial Quantity in Camellia oleifera Abel. Forests" Forests 14, no. 5: 982. https://doi.org/10.3390/f14050982

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