1. Introduction
Solar greenhouses offer advantages such as a high land utilization rate, short production cycle, and high technical content. They are therefore suitable for crop production in the cold regions of northern China [
1,
2], and provide much higher yields and incomes than open field cultivation [
3,
4]. However, microclimate factors in greenhouses, such as the temperature, lightintensity, humidity, and aeration, and management methods, including tillage and fertilization, can give rise to soil acidification, secondary salinization, and nutrient enrichment and unbalance [
5,
6,
7,
8].
The tomato, a vegetable cultivar native to western South America, has been widely cultivated in China since the 1950s, due to its high yield and rich nutrition [
9,
10]. In 2014, the tomato cultivated area in the Liaoning Province was 850 million square meters, of which 75% was protected cultivation area. Continuous monoculture of tomato is more common in protected cultivation than in non-protected cultivation [
11]. However, the continuous cropping of a single species leads to several soil-related obstacles [
12,
13], manifesting as retarded plant growth, serious pest and disease damage, low crop productivity, and soil degradation [
14,
15]. Numerous studies have asserted that the mechanisms of these obstacles mainly include changes in soil physicochemical properties, destruction of the ecological environment, and plant autotoxicity [
16,
17]. Over the past several years, many researchers have attempted to determine how to eliminate these obstacles through improving cultivation and management methods. Most research has focused on screening superior varieties to alleviate pests and disease, introducing grafting techniques to enhance plant resistance, applying organic fertilizer to improve soil quality, or selecting alternative rotations to balance soil nutrition [
18,
19,
20]. However, the changes in soil quality due to continuous monoculture over several years or crops have been rarely reported. In addition, the relationships between soil microbial properties, soil enzyme activities, and continuous tomato monoculture in solar greenhouses, remain poorly understood.
Soil microorganisms play vital roles in soil ecosystems, dominating the cycling of nutrients, the decomposition of organic matter, and the maintenance of soil fertility [
7,
21,
22,
23]. The total microbial abundance is a basal indicator of soil quality [
24]. Over years of continuous cropping, the abundance of soil bacteria first decreases and then increases, whereas the abundance of fungi increases [
25]. Increasing evidence indicates that an appropriate community population, abundant diversity, and high microbial activity, are all important factors for maintaining the sustainability and productivity of soil ecosystems [
26,
27]. In addition, a long-term field experiment revealed that the level of SMC functional diversity was significantly enhanced in plots treated with both chemical fertilizer and compost, compared with that in plots treated with only chemical fertilizer or in untreated control plots [
28].
The enzyme activity in the soil is another potentially sensitive indicator of soil quality. It is indicative of soil quality changes that occur due to management practices, and it can also be used to monitor soil microbial activity that is related to nutrient transformation [
29,
30]. Xiao et al. concluded that the activities of soil invertase, urease, and alkaline phosphatase were promoted in an intercropping system, when compared with those in a monoculture cropping system, and that the stimulation of urease and alkaline phosphatase activity from intercropped garlic was maintained until the garlic harvest [
31].
In the present study, to further understand soil microbial properties under different tomato monoculture crops, a Biolog EcoPlate was adopted to study the SMC functional diversity. The EcoPlate is based on the carbon substrate utilization by microbial communities, and the resulting data are analyzed via multivariate statistics, including principal component analysis (PCA) and the analysis of microbial community dynamics [
32,
33]. In this study, soil was analyzed to determine the microbial parameters, chemical properties, and enzyme activity under different continuous monoculture crops in a solar greenhouse. This study increases our understanding of the changes in soil enzyme activity, soil chemical properties, SMC functional diversity, and tomato yields under continuous tomato monoculture crops in a solar greenhouse, and it provides insight into the crop at which the continuous cropping obstacles emerge due to continuous cropping. This study also provides a theoretical basis for the remediation of soil and fertilization during tomato cultivation under continuous monoculture in solar greenhouses.
4. Discussion
Soil microbes play essential roles in crop growth. The seedling age was assumed to be an important influence on the microbial activity and diversity in the rhizosphere soil of plants [
38]. Corneo et al. indicated that the most abundant and balanceable type of microflora in healthy soils was bacteria, followed by actinomycetes, and then fungi [
39]. Our study demonstrated that the total soil microbial abundance, bacterial abundance, B/F value, and SMC functional diversity indicators, initially increased and then gradually decreased with the increase of continuous monoculture crops in a solar greenhouse. Fungal abundance followed an N-type trend with the increase in crop number. The changes in soil microbial abundance and SMC functional diversity indicators suggested that short-term (less than seven or nine crops) continuous monoculture was beneficial to soil microbial accumulation and SMC functional diversity promotion. However, long-term continuous monoculture decreased microbial accumulation and SMC functional diversity. Similar trends have been reported in other crop species. Recent studies found that the SMC diversity in rhizosphere soils increased under short-term (less than 5–10 years) continuous cotton cropping, but decreased under long-term (more than 15–20 years) cropping [
40]. In addition, with increasing years of continuous cucumber cropping, the abundance of bacteria and total microbes followed a trend with an inverted saddle-shaped curve, and fungal abundance appeared to increase linearly [
41]. The most likely reasons for the above results are as follows: short-term continuous monoculture is beneficial to soil ripening, and the process of soil ripening promotes an increase in SMC functional diversity. Furthermore, short-term continuous monoculture is less likely to have negative effects on soil and tomato yields than long-term continuous monoculture. Conversely, long-term continuous monoculture changes the soil predominant microbes which appear as a significant increase of fungi abundance, and this may lead to soil problems and limit continuous crops.
The deterioration of soil chemical characters is considered a main cause of soil sickness [
42]. In our study, the soil pH, organic matter, available nitrogen, and available phosphorus at the 13th crop, were all significantly lower than they were at the 5th, 7th, and 9th crops. These results show that long-term continuous monoculture accelerated the deterioration of soil chemical characters. Moreover, the relationship analysis showed that soil total microbial abundance and bacterial abundance were both significantly positively correlated with soil organic matter and available potassium content. The soil AWCD value at 144 h was significantly and positively correlated with available potassium and available nitrogen content after several continuous monoculture crops. Previous studies have indicated that soil nutrient content regulates soil microbial properties, and the importance of soil nutrient content in shaping microbial properties has been reported by several studies [
43]. Therefore, we conclude that changes in soil chemical properties that occur under continuous cropping may lead to changes in soil microbial characteristics.
In our study, the activities of urease and invertase first increased and then gradually decreased under continuous monoculture. The neutral phosphatase activity observed at the 13th crop was significantly lower than the activities at the other crops. In addition, catalase activity decreased gradually with continuous monoculture crops. Our results are consistent with those of Lu et al., who concluded that continuous cotton monoculture initially enhanced soil urease and invertase activities, which peaked at 15 or 20 years, and then decreased as monoculture continued [
44]. However, our results of soil enzyme activity change under continuous cropping differ from those of other studies. For instance, Sun et al. found that the activities of soil phosphatase, saccharase, and urease decreased each year under continuous peanut cropping [
45], and Xiong et al. found that long-term continuous monoculture led to obvious declines in soil enzymatic activities and bacterial abundance [
17]. These among-study differences may be attributed to the following factors: different species or crops have different responses to continuous monoculture, such that changes in soil enzyme activity are inconsistent among studies [
14]. In addition, the quality of the naïve soil used for continuous monoculture differs among studies. Several agricultural practices, such as fertilization and irrigation of poor- or medium-quality soil, could improve soil activity under short-term continuous monoculture. However, long-term irrigation, fertilization, and continuous monoculture patterns would cause secondary soil problems, which may indirectly lead to a decrease in enzyme activity [
44].
Soil enzymes, which mainly originate from microorganisms and plants, are closely associated with soil microorganisms [
46]. For example, the activities of soil catalase and alkaline phosphatase are highly correlated with the soil microbial biomass [
47]. Mungai et al. concluded that SMC functional diversity had decisive effects on soil enzyme activity [
48]. Soil invertase was associated with both soil microbial biomass and the soil microbial population [
49]. In our study, the correlation analysis confirmed that the urease and invertase activities were strongly and positively correlated with the AWCD value at 144 h, in terms of SMC functional diversity, total soil microbial abundance, and bacterial abundance. Furthermore, the neutral phosphatase activity was strongly and positively correlated with SMC functional diversity, and the soil enzyme activities were negatively correlated with fungal abundance and actinomycete abundance. The correlation analysis demonstrated that the soil enzyme activities were closely associated with the soil microbial abundance and SMC functional diversity under the different continuous monoculture crops. Future studies will focus on the correlations between the diversity of the fungal or bacterial community structure and soil enzymes under different crops, under continuous monoculture in solar greenhouses.
5. Conclusions
In this study, traditional physiological and biochemical methods, and Biolog Eco microplates analysis technology, were adopted. Our findings indicated that continuous monoculture of tomato in a solar greenhouse led to changes in soil properties and affected the tomato yield. The results showed that short-term continuous monoculture of tomato for fewer than seven or nine crops, accelerated soil ripening and increased the tomato yield, whereas long-term continuous monoculture of tomato, i.e., for more than 11 crops, had adverse effects on the soil quality and tomato yield. These results were likely observed because the long-term continuous monoculture of tomato and additional fertilizer application decreased the availability of nutrient elements and soil enzyme activity, and led to the change in soil microorganism diversity and a decline in the tomato yield. Future research is required to evaluate the genetic and structural diversity of soil microorganisms for tomato crops under continuous monoculture, by performing high throughput sequencing analysis. Such analyses will provide theoretical support for the development of sustainable soils for protected crops under continuous monoculture.