Abstract
The medicinal value of the Ferula L. has been recognized for more than a thousand years. Wild stocks of Ferula have declined dramatically because high economic value has led to overharvesting. The objective of this study was to compare the rhizosphere microbial community of four Ferula species [F. syreitschikowii K.-Pol., F. gracilis (Ledeb.) Ledeb., F. ferulaeoides (Steud.) Korov., and F. lehmannii Boiss.] in the northern part of **njiang, China. The 16S rRNA sequences of rhizosphere bacteria were obtained with an Illumina paired-end sequence platform. Analysis was conducted to determine the richness and diversity of the rhizosphere bacterial communities. Two-way ANOVA indicated that plant species and soil depth had no significant effect on the alpha diversity of rhizobacteria. Linear discriminant analysis effect size showed that F. lehmannii followed by F. ferulaeoides had the most biomarkers and the highest taxon level, F. syreitschikowii and F. gracilis the least, while F. syreitschikowii and F. gracilis had the least property. This trend is consistent with reports that the medicinal value of F. lehmannii and F. ferulaeoides is greater than that of F. gracilis and F. syreitschikowii. The results of this study provide information that could be used for the commercial cultivation of Ferula spp.
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Introduction
Twenty-six Ferula species and one Ferula variant are present in China1. Twenty of these species are found in the ** histories and environmental conditions. Microbial Ecology 68, 794–806 (2014)." href="/article/10.1038/s41598-018-22802-y#ref-CR37" id="ref-link-section-d262096482e1078">37,38. Two-way ANOVA indicated that Ferula species significantly affected the relative abundance of Actinobacteria (P < 0.01), Gemmatimonadetes (P < 0.01), Bacteroidetes (P < 0.01), Acidobacteria (P < 0.01), Verrucomicrobia (P < 0.05) and Thaumarchaeota (P < 0.01). Soil depth significantly affected the relative abundance of Proteobacteria (P < 0.05), Acidobacteria (P < 0.05), Firmicutes (P < 0.05) and Verrucomicrobia (P < 0.01).
Figure 2b shows the top ten bacterial classes in the rhizosphere soil. Gammaproteobacteria had the highest abundance (15.28%), followed by unidentified_Gemmatimonadetes (8.90%) and Thermoleophilia (8.89%). The relative abundance of unidentified_Gemmatimonadetes (P < 0.01), Thermoleophilia(P < 0.05), unidentified_Acidobacteria (P < 0.01), unidentified_Actinobacteria (P < 0.05), Acidimicrobiia (P < 0.01), Cytophagia (P < 0.05) and Sphingobacteriia (P < 0.01) were significantly affected by Ferula species. The abundance of Sphingobacteriia was significantly affected by soil depth (P < 0.01).
Soil Physicochemical Properties
Soil physicochemical properties vary among soil types and with soil depth. Therefore, we measured 12 common soil physiochemical properties (Table S1) and then analyzed the correlation between these properties and the relative abundance of bacteria at the phylum and class levels. Two-way ANOVA indicated that Ferula species and soil depth significantly affected all 12 Soil physicochemical properties (P < 0.01).
By factor analysis, we reduced 12 physicochemical factors to 4 principal components. The results of the correlation analysis of these four components with the relative abundance of bacteria in the rhizosphere are shown in Table S2 (phylum level) and Table S3 (class levels). We found that 12 physicochemical factors in rhizobacteria also have an impact on each other. For example, nitrate nitrogen and ammonium nitrogen are closely related, and they have impact on certain bacteria consistently.
Overall, these results suggest that soil properties were positively correlated with the relative abundance of bacteria.
Alpha Diversity
Alpha Diversity is used to analyze the diversity of species within community samples39. In general, sequences with greater than 97% identity are clustered into one operational taxonomic unit. The Alpha Diversity analysis index for different samples at a 97% identity are shown in Table 2. Two-way ANOVA indicated no significant differences among soil samples in observed species, Shannon, Simpson, Chao1, and ACE. Good’s coverage ranged from 97 to 98%, indicating that the measurement depth has met the requirements.
In summary, we propose a hypothesis that the reason that some of the soil bacteria are sensitive to soil depth and medicinal value is that these microorganisms are sensitive to volatile oil from plant.
As the rhizosphere soil volatile substances can not only come from the roots, but also from the ground parts of Ferula. For example, shoots can emit volatile substances in gaseous form which can diffuse into the surface soil, the rainwater can dissolve the volatile material to bring it into the soil. These processes gradually become less pronounced with the soil depth increased. So the abundance of some volatile-sensitive bacteria is higher in the upper soil (3 cm) and lower in the deeper soil (20 and 40 cm).
The results of LEfSe suggest that Ferula species with greater medicinal efficacy have a more unique microbial community (biomarkers) in the rhizosphere. The likely reason is that Ferula species with high medicinal efficacy produce more and better Ferula gum and volatile substances than species with low medicinal efficacy. That is to say, the medicinal value of Ferula is closely related to this volatile substance. The more volatile material the flavor has, the higher medicinal value is. We hypothesize that the differences in microbial populations among Ferula species were primarily due to differences in the production of volatile substances which can increase microbial diversity and abundance.
One shortcoming in our study is that the four Ferula species in this study were collected from areas which differed in geographical environment and climatic conditions. Ecological and geographical conditions greatly influence the terpenoid content of Ferula plants43. Therefore, the plant species factor in this study also includes the effects of the different environments in which the plants were growing. However, it is rare to find two Ferula species in the same field. We are not aware of any places where Ferula is being cultivated, so we could not obtain Ferula plants that had been grown under identical conditions. Each Ferula species has its unique habitat. Thus to a certain extent, the four Ferula species represent the environment in which they were growing.
Previous studies have examined the rhizosphere microbial community of F. sinkiangensis and F. fukanensis24,25. This study was the first to describe the rhizosphere microbial community of F. syreitschikowii, F. gracilis, F. ferulaeoides, and F. lehmannii. Many studies have compared the rhizosphere microbial community among species within a genus. Liu proposed that tree species influenced microbial diversity and nitrogen availability in rhizosphere soil44. Ladygina and Hedlun observed that plant species influenced microbial diversity and carbon allocation in the rhizosphere soil45. Cleary reported that root depth and plant species influenced microbiological parameters and bacterial composition in a mercury contaminated salt marsh46.
In conclusion, the results indicate that soil depth had some effect on bacterial community structure. And some rhizosphere bacteria are sensitive to soil depth and medicinal value of Ferula. The abundance of specific rhizosphere bacteria become higher as the medicinal value of the Ferula species increased and the soil depth decreased. This discovery provides insight about the ecological characteristics of Ferula. More information is still needed, but perhaps we can increase the survival rate of cultivated Ferula by artificially increasing the abundance of certain microorganisms.
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Acknowledgements
This work was financially supported by the Chinese National Basic Research Program (2014CB954203) and the National Natural Science Foundation of China (31360139, 41561010, 31560177).
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Professor Li Zhuang and **uling Wang designed the experiment. **uling Wang and Zhongke Wang analyzed the data. **uling Wang and ** Jiang wrote the article. Yaling He, Yudi Mu and **nhua Lv modified the article. **uling Wang collected the samples.
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Wang, X., Wang, Z., Jiang, P. et al. Bacterial diversity and community structure in the rhizosphere of four Ferula species. Sci Rep 8, 5345 (2018). https://doi.org/10.1038/s41598-018-22802-y
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DOI: https://doi.org/10.1038/s41598-018-22802-y
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