Effect of pepper and cabbage planting on loess of Guyuan region of China on microbial diversity

doi:10.21203/rs.3.rs-2720754/v1

Diversity of microorganisms in loess plateau plays critical role in improvement of soil quality. One good strategy is that planting crop improves community of soil microorganisms; however, how microorganism diversity is affected by crop remains unclear. Here, we used a sequencing technology to study the effect of pepper and cabbage crops on soil microorganisms in loess of Guyuan region of China. The analysis revealed that both cabbage and pepper increase the specific Operational Taxonomic Units (OTUs) in soil and diversity of microorganisms was enhanced after cabbage and pepper were cultivated. Ascomycota are the primary fungus species of the soil, and inhibited significantly with the increased soil layers by pepper and cabbage. Contrarily, the development of Actinobacteria is improved and no new microbial species were found with the increased soil layers when pepper and cabbage were planted. (These data indicate that pepper and cabbage promote more reasonable microbial community of the deep soil layer. We speculate that deep ploughing may be a good planting strategy for crop growth in loess plateau. These findings will provide an insight for the improvement of soil quality in the Guyuan region of China.

Pepper

Cabbage

Microorganism

Diversity

Soil

Loess plateau of Guyuan region located in northwest China is known as a hot-spot region of studying microbial community diversity and assessing soil quality(Jia, et al. 2020). Understanding the characteristic of the soil microbiome and how their community and component are changed by crop is important and crucial, which can be significant for developing a sustainable ecosystem in soil microorganisms. Microorganisms are active components in the soil structure, which include species that have various effects on plant nutrition and health(Crits-Christoph, et al. 2018; Chen, et al. 2019). Meanwhile, plants also actively regulate microbial distribution by secretion of root exudates(Badri and Vivanco 2009; Song, et al. 2021). The amount and type of plant root exudates are species-specifc, which contributes to the influence of plant species identity on microbial communities(Steinauer, et al. 2016; Pang, et al. 2021). The surrounding mass of soil is a breeding bank for microbes that can be selected by growing plant roots. Therefore, there is an ecological cycle of root-microorganism in soil(Gao, et al. 2022; Li, Xie, et al. 2022). The composition and functionality of microorganism communities are changed, updated and utilized continually by the dynamic circulation between soil and plant.

Soil microorganisms usually infect host plants asymptomatically and reside within the tissues of living plants(Wang, et al. 2017). Some species of microorganisms increase the fitness of host plants by enhancing their resistance to abiotic and biotic stresses (Barrow and Lambers 2022; Chamkhi, et al. 2022). Currently, considerable research is being conducted on plant response to microorganisms and metabolite bio-activity of microorganisms to understand the relationship between soil microorganisms and their host plants, while there is little information on how microorganism communities change when living under the conditions of crop planting. The certain evidence suggests that this may occur in the roots of plants. Sall et al. (2006) showed that the community diversity of microorganism are higher in cultivated soil than in fallow(Sall, et al. 2006). Soil quality was significantly improved due to the enhancement of soil microbial diversity(Nautiyal, et al. 2010). Wu et al. (2022) reported that temporal variation and enrichment in the diversity of microorganisms was changed with the depth of soil layer, which also suggests the importance of soil tillage depth to the nutritional requirements of the plant(Wu, et al. 2022). This conclusion also is further confirmed by the study of Li et al. (2013), who found that soil microbial biomass increased with soil depth(Li, et al. 2013). Thus, in conclusion, the variation trend of soil microbial community after plant planting has a certain regularity.

Based on the above research results, we hypothesize that: (1) the community structure of microorganisms in the soil exhibit a regular change along with change of soil depth; (2) plant cultivation affects the distribution of soil microorganism community; and (3) the soil planting different cropa may change microorganism community . Here, we selected the pepper and cabbage as the main horticultural crops planted in Guyuan region to explore their effects on microbial diversity. Our study will provide an insight for the mechanism by which the interaction between soil microorganism and plant is understood further.

2.1.Sample collection

Pepper and cabbage crops were planted from May 10 to August 1, 2022 in Guyuan City, Ningxia Province, China (E 106.28°, N 36.01°). After the planting period is over, the soil were sampled from the 0~20 cm and 20~40 cm layers of soil planting pepper and cabbage. Each sample consists of soil equable mixture from seven soil points of each site. Briefly, after sampling, Residual plant organs/tissues are removed from the soil and samples are for preservation in 4℃ of freezer. The control soil was collected from the mixture of 0~20 cm and 20~40 cm layers of soil in no crop-cultivated land.

2.2. Sequencing of amplicon

A FastDNA Spin kit for soil (MP, M5635-02, USA was used to extract total community genomic DNA, and the extracted DNA was further purified using the DNA purification kit (Yeasen Biotechnology Co., Ltd., China). Then, specific primers (16S V4: 505F/806R, ITS1/ITS2) was used to amplify 16S rRNA and ITS genes (Table S1). All PCR reactions were carried out using the following program: initial denaturation at 98℃ for 1 min, followed by 30 cycles of denaturation at 98 ℃ for 10 s, annealing at 50℃ for 30 s, and elongation at 72℃ for 30 s, and final extension at 72℃ for 5 min.

PCR products from each sample were mixed in equidensity ratios and purified with Qiagen Gel Extraction Kit (Qiagen, Germany). Sequencing libraries were generated using TruSeq ® DNA PCR-Free Sample Preparation Kit (Illumina, USA). Finally, the library was sequenced on an Illumina NovaSeq platform to generate the paired-end reads.

2.3. Data analysis

The paired-end reads were assigned to samples and merged using FLASH (V1.2.7, http://ccb.jhu.edu/software/FLASH/), which merges the reads when the correct overlap is found; the splicing sequences were called the raw tag. Quality filtering on the raw tags was performed using QIIME (V1.9.1, http://qiime.org/scripts/split_libraries_fastq.html) under specific filtering conditions to obtain high-quality clean tags. The tags were then compared with the reference database (Silva database (16S/18S), https://www.arb-silva.de/; Unite Database (ITS), https://unite.ut.ee/) using UCHIME Algorithm (http://www.drive5.com/usearch/manual/uchime_algo.html) to detect and remove the chimera sequences and finally obtain the effective tags.

Sequences analysis was performed using the Uparse software (Uparsev7.0. 1001, http://drive5.com/uparse/). Sequences with ≥97% similarity were assigned to the same Operational Taxonomic Units (OTUs). For each representative sequence of 16S and ITS, using the Silva Database (http://www.arb-silva.de/) for taxonomic annotationd. The representative sequence for each OTU was screened for further annotation. Multiple sequence alignment was performed using the MUSCLE software (V3.8.31, http://www.drive5.com/muscle/). OTUs abundance information was normalized using a standard of sequence number corresponding to the sample with the least sequences. Alpha diversity and Beta diversity were measured using the QIIME software (V1.9. 1) to assess and evaluate the differences in microbial species complexity. Principal Component Analysis (PCA) analysis based on OTU level. Linear discriminant analysis (LDA) effect size (LEfSe) was applied to identify different microbiota characteristics using LEfSe software; the threshold on the logarithmic LDA score for discriminative features was 2.0. graphviz-2.38.0 software was used to draw the network diagram.

3.1.Species annotation and alpha diversity analysis

A total of 6 composite samples, including 3 soil fungi (G, H and Q groups) and 3 soil bacteria (L, K and J groups) samples (with three biological replicates per sample), were subjected to high-throughput sequencing using the Illumina NovaSeq system. A total of 1542728 raw reads and 1438245 effective tags, including 764899 raw reads and 724099 effective tags from cabbage-cultivated soil microorganism (average: 84989 reads per sample) and 777829 raw reads and 714146 effective tags from pepper-cultivated soil microorganism (average: 864265 reads per sample). Based on the least number of sequences detected among the assayed samples, we randomly selected and compared 80455 and 79350 effective reads of cabbage-cultivated soil microorganism and pepper-cultivated soil microorganism per sample. Results from Fig. 1AC divulged that 512, 655, 723 fungus total OTUs as soon as 5524, 5334 and 5301 bacteria total OTUs were identified in control (G), 0~20 cm (H) and 20~40 cm (Q), respectively. 698, 766, 757 fungus total OTUs were identified while 5373, 5671 and 5624 bacteria total OTUs of was observed in control (L), 0~20 cm (K) and 20~40 cm (J). This data suggests that cabbage and pepper increase the total fungus OTUs as comparison to the control, but the effect of the former on the fungus total OTUs from deep soil is more significant than the later (Table 1).

Table 1. Data preprocessing statistics and quality control statistics
Sample Name	Raw Tags	Clean Tags	Effective Tags	Effective%
G.1	93,862	93,262	88,860	93.04
G.2	80,537	80,014	77,791	94.95
G.3	83,209	82,719	77,140	90.82
H.1	87,112	86,664	83,051	93.95
H.2	80,365	79,916	76,825	93.46
H.3	83,718	83,258	79,329	93.77
Q.1	88,299	87,788	82,271	91.96
Q.2	82,140	81,630	76,204	90.55
Q.3	85,657	85,233	82,628	94.72
Subtotals	764,899	760,484	724,099
Average	84,989	84,498	80,455
L.1	87,589	86,784	68,828	78.19
L.2	81,029	80,641	76,255	92.59
L.3	87,058	86,679	82,701	94.42
J.1	91,492	91,053	81,935	89.3
J.2	90,893	90,430	85,243	92.37
J.3	87,872	87,373	82,288	93.15
K.1	83,667	83,257	77,891	91.27
K.2	79,009	78,653	75,016	94.01
K.3	89,220	88,730	83,989	92.98
Subtotals	777829	773600	714146
Average	86425	85956	79350
Totals	1542728	1534084	1438245

G, H, Q means these samples from the control, 0~20 cm soil layer and 20~40 cm layer in cab-bage-cultivated soil while L, K and J presented these samples from the control, 0~20 cm soil layer and 20~40 cm layer in pepper-cultivated soil, respectively. 1, 2 and 3 represent the repetition.

Cabbage decreased the bacteria total OTUs while pepper increased that. In addition, H and Q groups contained 158 and 226 fungus specific OTUs, and K and J groups contained 189 and 224 fungus specific OTUs. Similarly, H and Q groups contained 703 and 770 bacteria specific OTUs, while K and J groups contained 731 and 876 bacteria specific OTUs (Fig. 1AB), indicating that both cultivation of cabbage and pepper increase the specific OTUs in soil.

To determine whether the amount of sequencing data generated was reasonable we constructed dilution curves by plotting the amount of extracted data (y-axis) against the alpha diversity index (x-axis), which reflects the abundance and diversity of a given species in the sample (Fig. 1C). The alpha diversity index was determined the Shannon index, which is often used along with the observed_species to reflect the alpha diversity index; Similar, the greater the observed_species, the higher the community diversity (Fig. 2A). The larger the value of the Shannon index, the higher the community diversity (Fig. 2B). Our results showed the diversity of microorganisms was enhanced after cabbage and pepper were cultivated. Microorganism diversity of shallow soils is more abundant than that of deep soil in cabbage-cultivated soil, but the contrary results were observed in pepper-cultivated soil.

3.2. Beta diversity and phylogenetic information visualization

Analysis of weighted unifric and unweighted unifric is a non-parametric test used to test whether the differences between groups (two or more) are significantly greater than those within a group (Fig. 3AB). In addition, we also evaluated beta diversity at the level of OTUs, which were defined based on a similarity cut-of of 97%. To compare the composition of the identified microbial communities within different plant compartments, Bray-Curtis dissimilarity was performed at the OTU level. The smaller the P-value, the greater the significance of the differences between groups (Fig. 3CD). A statistically significant P-value (P<0.05) and change of weighted unifric and unweighted unifric after cabbage and pepper were planted indicates that the grouping is meaningful. Principal coordinate analysis (PCA) of measured samples showed that all groups were dispersed as comparison to the control (Fig. 3E).

Phylogenetic visualization analysis of the similarity among the fungus samples showed that excluding the unclassified OTUs, a total of 89 genera belonging to 8 families were identified, and 67 classes genera from Ascomycota family, and 14 classes is distributed into the Basidiomycota. Other classes only possessed a little percentage. Cladosporium from Ascomycota possessed the higher percentage than others in all groups, and percentage of Cladosporium was decreased significantly when cabbage and pepper were planted in measured groups (Fig. 4A). Phylogenetic visualization analysis of the similarity among the six samples showed that 100 genera belonging to 14 families were identified, and 38 classes is presented in Proteobacteria family. 16, 11 and 12 classes were distributed in Myxococcota, Synergistota and Actinobacteria families, respectively. Sphingomonas from Proteobacteria family and Pseudarthrobacter from Actinobacteria family possessed the higher percentage than other (Fig. 4B).

3.3. Correlation between the relative abundance of dominant species and collinearity

Fig. 5A shows the microbial species composition and relative abundance (mean relative abundance>1%) at the phylum level in fungus groups. Excluding unclassified and others, the six groups were mainly composed of fungi belonging to the phyla Ascomycota, Basidiomycota, Mortierellomycota and Chrytridiomycota, with the former three phyla representing the core fungal communities. In all measured groups, Ascomycota possessed the highest relative abundance of fungus than any other, suggesting Ascomycota is the primary fungus species in soil. However, Although Ascomycota was dominant at all groups, its relative abundance gradually decreased with the increased deep of soil. Contrarily, increased relative abundance in Mortierellomycota and others were observed. This revealed that pepper and cabbage weakened dominance of Ascomycota and promote the balance of fungal distribution with increased soil depth.

Fig. 5B shows the microbial species composition and relative abundance (mean relative abundance>1%) at the genus level in bacteria groups. The six groups were mainly composed of Proteobacteria, Actinobacteria, Bacteroidota, Myxococcota, Firmicutes, Acidobacteriota, Verrucomicrobiota, Synergistota, Fusobacteriota, Actinobacteriota, Gemmatimonadetes, Crenarchaeota, Chloroflexi and Gemmatimonadota. In all measured groups, Proteobacteria was the most dominant genus, followed by Firmicutes, Hygrocybe, Actinobacteriota, and Synergistota. Pseudarthrobacter from Actinobacteria was the most dominant genus, followed by Sphingomonas from Proteobacteria and Bacillus from Firmicutes. The relative abundance of these microbial species is decreased when cabbage and pepper were cultivated. This data suggests that pepper and cabbage weakened expression of some dominant bacteria and encouraged the development of other weak microbial communities.

3.4. Analysis of different flora and differentially expressed abundance

LEfSe is used to determine the genetic or functional features that best explain the differences between two or more groups of samples under different biological conditions or environments as well as the degree to which these features influence the differences between groups. Our results showed that Asmcomycota was the main fungal communities in cabbage-cultivated fungus groups (Fig. 6A); Mortierellomycota in pepper-cultivated fungus groups (Fig. 6B); Hymenobacteraceae in cabbage-cultivated bacteria groups (Fig. 6C); Firmicutes, and Acidobacteria in pepper-cultivated bacteria groups (Fig. 6D).

Expression abundance of 35 primary classes were further determined, and found that abundance of Cladosporium from Ascomycota is reduced among all species after when crops were planted. In addition, species of increased expression possessed more ratio than the control among measured fungus (Fig. 7A). Similar results also were observed in bacterial. No new species were observed in the measured microorganisms (Fig. 7B). The data indicated that as a whole cabbage and pepper promote the diversity to change the relative expression of microorganism but not to generate new species. In addition, 8 classes of fungus, including Mortierellomycota, Basidiomycota, Zoopagomycota, Ascomycota, Chytridiomycota, Rozellomycota, Basidiobolomycota and Aphelidiomycota, generate the interaction in measured soil. Ascomycota and Chytridiomycota showed the direct obvious interact relationship (Fig. 7C). The relationship also was observed between Ascomycota and Basidiobolomycota. 25 classes of bacteria showed the interaction relationship in soil. Except the unidentified species, Proteobacteria, Acidobacteria and Actinobacteria are the main species generating the interaction (Fig. 7D).

Soil microbial diversity is a potential indicator of soil quality and can predict changes in soil properties(Li, et al. 2020; Ameen, et al. 2021). Therefore, estimating the diversity of soil microbes helps determine the soil components and types of cultivated crops, thereby improving the inorganic constituents of soil that are easily absorbed by plants (Xu, et al. 2014; Amaral, et al. 2023). Soil enzymes produced by microorganisms transform the substrates via the cycles of plant-microorganism-soil(Loeppmann, et al. 2016; Schimel, et al. 2022). Thus, the characteristic of microorganism community has been significantly correlated with plant growth. In the current study, the community of the soil microorganisms were changed when cabbage and pepper were cultivated, and the changes in relative abundance of soil microbial were statistically different between the control and the treatments. This finding suggests that cabbage and pepper can promote the community balance of soil microbial by regulating their proportion in soil. Importantly, no new microorganism was generated and the specific OTUs were increased when these crops were cultivated. This information is important for arid or saline areas of Guyuan region where soil quality is improved by adding microbial fertilizers, which add new necessary microbial species and regulate the proportion of other specific species to promote the growth of pepper and cabbage.

Ascomycota is one of most diverse phyla of eukaryotes with at least 83,000 described species that represent more than half of all described species of fungi and known for their phenotypic diversity, including their extremotolerance and ability to grow on various carbon sources(Moustafa, et al. 2011; Stenroos, et al. 2019). Numerous studies have documented the fungal species belonging to Ascomycota are important saprobic or parasitical organisms that live on a wide range of organic substrates which infect plant tissue/organ to result in the happening of powdery mildew(Qiu, et al. 2019), anthracnose(Johnny, et al. 2011), disease etc. (Charron, et al. 2018). In the current study, we found that Ascomycota are primary the type of fungus in soil, but its relative abundance is significantly decreased with increased soil depth when cabbage and pepper were cultivated, suggesting that cabbage and pepper may reduce the risk of plant infection by some species from Ascomycota. There are other beneficial divergent genera, such as Mortierellomycota. The latest results in 2021 show that some species of (Xu

2021). This may be related to root characteristic of cabbage and pepper. As tap root system, the roots of cabbage and pepper can reach to deeper soil layer, thereby inhibiting or promoting the growth of some microorganism by secreting some inhibitors (Yeoung, et al. 2002; Sharma, et al. 2011), such as proteinaceous xylanase inhibitors(Chmelova, et al. 2019), furfural, acetic acid, and syringaldehyde(Wang, et al. 2022). Our data speculated that pepper and cabbage could improve soil quality by regulating soil microbial community.

Analysis of relative abundance and LEfSe showed that Proteobacteria, Actinobacteria and Firmicutes play a key role in bacteria community, and proportion in soil was changed and no new species were produced when cabbage and pepper were cultivated. Interestingly, the relative abundance of Actinobacteria is increased with increased soil later after pepper and cabbage were cultivated. The metabolic activities of Actinomycetes can promote the decomposition of organic materials and refine them into available phosphorus and nitrogen that can be directly absorbed and utilized by crops(Li, Sun, et al. 2022). Actinomycetes can improve soil physical properties, increase soil water-stable aggregate structure, reduce bulk density, and increase air permeability(Ghorbani, et al. 2013; Karkouri, et al. 2019; Li, Sun, et al. 2022). Our results indicated that pepper and cabbage only affect the diversity microorganism by changing their proportion in soil, and deep soil layer may be more helpful of plant growth.

This study evaluated the effect of pepper and cabbage planting on loess of Guyuan region of China on microbial diversity and found that deep soil layer was suitable for crop cultivation. The deep soil layer had more reasonable microbial community due to the change in the relative abundance of microorganisms after pepper and cabbage were planted. Further, we identified Ascomycota are the primary fungus species of the soil, and inhibited significantly by pepper and cabbage. Contrarily, pepper and cabbage promote the development of Actinobacteria. Interestingly, no new microbial species were found when pepper and cabbage were cultivated. We speculate that deep ploughing may be a good planting strategy for crop growth in loess plateau. These findings will provide a basis for planning strategies to the improvement of soil quality in the Guyuan region of China.

Ethics approval and consent to participate: Not Applicable.

Consent for publication: Not Applicable.

Competing interests: The authors declare no competing interests.

Authors' contributions：Z.X. and wrote the main manuscript text. H.Y. and C.G. prepared figures 1-7. All authors reviewed the manuscript..

Availability of data and materials: not applicable.

Acknowledgments

This research was funded by National Key Research and Development Project of China (No. 2021YFD1600302), Nature and Science Foundation of Ningxia (2022AAC05023), and Key Research and Development Plan (Major Projects) of Ningxia (NXNYYZ202001).

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No competing interests reported.

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Effect of pepper and cabbage planting on loess of Guyuan region of China on microbial diversity

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Abstract

Figures

1. Introduction

2. Materials And Methods

3. Results

4. Discussion

5. Conclusion

Declarations

References

Additional Declarations

Supplementary Files

Status:

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