Abstract
Background
The most serious challenges in medicinal ‘Sanghuang’ mushroom production are the fungal diseases caused by various molds. Application of biological agents has been regarded as a potential crop disease management strategy. Here, the soil microbiome associated with ‘Sanghuang’ mushroom affected by fungal diseases grown under field cultivation (FC) and hanging cultivation (HC) was characterized using culture-dependent and culture-independent methods.
Results
A total of 12,525 operational taxonomic units (OTUs) and 168 pure cultures were obtained using high-throughput sequencing and a culture-dependent method, respectively. From high-throughput sequencing, we found that HC samples had more OTUs, higher α-diversity, and greater microbial community complexity than FC samples. Analysis of β-diversity divided the soil microbes into two groups according to cultivation mode. Basidiomycota (48.6%) and Ascomycota (46.5%) were the two dominant fungal phyla in FC samples, with the representative genera Trichoderma (56.3%), Coprinellus (29.4%) and Discosia (4.8%), while only the phylum Ascomycota (84.5%) was predominant in HC samples, with the representative genera Discosia (34.0%), Trichoderma (30.2%), Penicillium (14.9%), and Aspergillus (7.8%). Notably, Trichoderma was predominant in both the culture-independent and culture-dependent analyses, with Trichoderma sp. FZ0005 showing high host pathogenicity. Among the 87 culturable bacteria, 15 exhibited varying extents of antifungal activity against Trichoderma sp. FZ0005, with three strains of Bacillus spp. (HX0037, HX0016, and HX0039) showing outstanding antifungal capacity.
Conclusions
Overall, our results suggest that Trichoderma is the major causal agent of ‘Sanghuang’ fungal diseases and that Bacillus strains may be used as biocontrol agents in ‘Sanghuang’ cultivation.
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Introduction
A precious basidiomycete fungus, Inonotus baumii (formerly Phellinus baumii), has been widely utilized in China, Japan and other Asian countries as a traditional Chinese medicinal mushroom [1, 2]. In China, I. baumii is commonly called ‘Sanghuang’ mushroom, a yellow fungus that grows on mulberry. It is regarded as being advantageous to human health due to its high biological activities, including antitumor, anti-inflammation, and antioxidation effects [3,4,5]. Numerous studies have documented that natural compounds such as polysaccharides, flavones, and ergosterol are the bioactive metabolites responsible for the medicinal and gastronomic value of ‘Sanghuang’ [6, 7]. In recent years, indoor artificial cultivation of ‘Sanghuang’ mushroom has been developed and practiced on a large scale in China [58,59]. For hosts, microbial communities are an important line of defense against pathogenic microorganism invasion from the environment [60, 61]. Numerous studies have demonstrated that the health status of a host (e.g., plant or mushroom) is a result of complex interactions between the host, the soil environment, and microorganisms, including pathogens and other microorganisms in the soil or within the plant, indicating that the richer and more diverse the microbial community in the habitats of the host is, the more complex the interspecific interactions, and the stronger the ability of the host to resist invasion by external pathogenic microorganisms [62,63,64]. Our findings indicated that HC samples had more OTUs, higher α-diversity, and greater microbial community complexity than FC samples. Analogous to findings for other hosts [13, 65], we speculated that there were connections between the microbial community structure and growth status of ‘Sanghuang’ mushroom.
With the emergence of limitations in traditional control methods for host diseases (e.g., chemical control and resistance breeding), the current methods of biological control for host diseases involving a search for natural antagonistic microorganisms have attracted widespread attention [43]. In recent years, the application of Bacillus and Pseudomonas as biocontrol strains has been studied in depth [66, 67]. Chen et al. [68] reported that Bacillus subtilis 151B1 and YBC could be used as potential biological agents to control passion fruit disease caused by Fusarium solani. Ren et al. [69] revealed that Pseudomonas poae JSU-Y1 had the potential to control the growth of toxigenic fungi in agricultural products. Our collection of bacteria antagonistic to Trichoderma also included members of Bacillus and Pseudomonas. Furthermore, we also performed a screening experiment of antagonistic bacteria against Fusarium, and the study showed that the antagonistic bacteria also included Bacillus with a good antifungal effect (data not shown). Notably, Bacillus spp. (HX0037, HX0016, and HX0039) exhibited outstanding inhibitory activity against Trichoderma FZ0005, suggesting that they might serve as potential biological resources for the biocontrol of ‘Sanghuang’ diseases. As reported in other studies, the use of biofungicides based on Bacillus species could be regarded as a biological alternative to synthetic fungicides employed in mushroom production [20, 70]. We suggest that a bacterial suspension of Bacillus strains with antifungal activity against Trichoderma FZ0005 should be sprayed onto the cultivation soil or the surface of bag-cultivated ‘Sanghuang’ mushrooms during propagation and at the stage of fruiting body formation. Moreover, adding beneficial Bacillus (HX0037, HX0016, and HX0039) bacteria to water tanks used for daily irrigation might provide an additional strategy for disease management. The biocontrol activity and mechanism of these antagonistic bacteria, however, remain to be further characterized. According to our findings, we hypothesized that Bacillus occupied a dominant ecological niche in the soil microbiome of HC, which not only stabilized the soil microecosystem but also effectively antagonized the major pathogen causing the fungal diseases of ‘Sanghuang’, thereby possibly reducing the production of mold conidia released into the air.
Conclusions
High-throughput sequencing technology and traditional culture-dependent methods were used to analyze the structure of soil microbial communities of ‘Sanghuang’ mushroom suffering from fungal diseases. Our results revealed that cultivation mode could influence the structure of soil microbial communities of ‘Sanghuang’ mushroom, and the Trichoderma genus was the major causal agent of ‘Sanghuang’ fungal diseases. Three Bacillus spp. (HX0037, HX0016, and HX0039) exhibited effective antifungal activity against Trichoderma sp. FZ0005 and might be useful as future biocontrol agents against fungal diseases affecting ‘Sanghuang’ mushroom.
Data Availability
All data are available upon request to the corresponding author. Complete culture-independent sequence datasets were submitted to the NCBI Sequence Read Archive (SRA) database under the accession number SRP395845 (ITS) and SRP395839 (16 S rDNA), respectively. The data can be found at https://www.ncbi.nlm.nih.gov/sra/?term=SRP395845 (ITS) and https://www.ncbi.nlm.nih.gov/sra/?term=SRP395839 (16 S rDNA). The ITS gene sequences of the culturable fungal isolates were submitted to GenBank under the accession numbers OP269747-OP269827. The 16 S rDNA sequences of the culturable bacterial isolates were submitted to GenBank under the accession numbers OP268496-OP268582. All data generated or analyzed during this study are included in this article and its supporting information files.
Abbreviations
- FC:
-
Field cultivation
- HC:
-
Hanging cultivation
- OTUs:
-
Operational taxonomic units
- EC:
-
Electrical conductivity
- AN:
-
Available nitrogen
- AP:
-
Available phosphorus
- AK:
-
Available potassium
- PCR:
-
Polymerase chain reaction
- WA:
-
Water agar
- GA:
-
Gause’s agar
- PDA:
-
Potato dextrose agar
- PCoA:
-
Principal coordinate analysis
- PERMANOVA:
-
Permutational multivariate analysis of variance
- Di:
-
Diameter of the fungal inhibition zone
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Acknowledgements
The authors are sincerely grateful to Prof. Jie **e (Southwest University, Chongqing, China) and Dr. **aojiao Liu (Southwest University, Chongqing, China) for their critical review and editing of this manuscript. Help from Shaoxin Qin (**zhai Shangzhen Biotechnology Co., Ltd.) and Tao Xu (**zhai Shangzhen Biotechnology Co., Ltd) in ‘Sanghuang’-related material collection is greatly appreciated. We are very grateful to Wekemo Tech Group Co., Ltd., Shenzhen, China, for technical support with sequencing and data analysis.
Funding
The authors acknowledge the financial support from the Anhui Provincial Natural Science Foundation (Grants 2108085QH374), Fundamental Research Funds for the Anhui University of Chinese Medicine (Grants 2020rcyb008), and Foundation of Anhui Province Key Laboratory of Research & Development of Chinese Medicine (Grants AKLPDCM202310) to Weifang Xu and the Academic Funding for Top Talents in Disciplines (Specialties) of Anhui Provincial Higher Education Institutes (Grants gxbjZD2021056) to Dengke Yin.
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W.X. and D.Y. designed this study. W.X., J.D. and Y.Z. contributed to collecting samples; T.S., S.J., Y.Z., G.B., and W.L. performed the experiments; T.S. wrote the original manuscript text; W.X., T.S., J.D. and S.J. reviewed and edited the writing; W.X. and D.Y. supplied the funding. All authors have read and agreed to the published version of the manuscript.
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Supplementary Material 1: Table S1 High-throughput sequencing statistics of soil samples of ‘Sanghuang’ mushroom. Table S2. α-Diversity index of soil samples from the high-throughput sequencing data. Table S3. PERMANOVA results from the high-throughput sequencing data. Table S4. Correlation network analysis of soil microbial communities from the high-throughput sequencing data. Table S5. Distribution of culturable fungi isolated from the soil of ‘Sanghuang’ mushroom. Table S6. Relative frequency of culturable fungi in the soil samples grown under different cultivation modes of ‘Sanghuang’ mushroom. Table S7. Distribution of culturable bacteria isolated from the soil associated with ‘Sanghuang’ mushroom. Table S8. Relative frequency of culturable bacteria in the soil samples grown under different cultivation modes of ‘Sanghuang’ mushroom. Fig. S1 Pathogenicity determination of the pathogenic fungus Trichoderma FZ0005. Fig. S2 Correlations between soil physicochemical properties and total soil microbial taxa associated with ‘Sanghuang’ mushroom. Fig. S3 Composition of soil bacterial communities of ‘Sanghuang’ mushroom. Fig. S4 Colony features of some culturable soil microbes and electrophoretograms of their PCR products. Fig. S5 Comparison of genus-level microbial composition between culture-dependent and culture-independent methods. Fig. S6 Screening of partial antagonistic strains against Trichoderma sp. FZ0005.
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Xu, W., Sun, T., Du, J. et al. Structure and ecological function of the soil microbiome associated with ‘Sanghuang’ mushrooms suffering from fungal diseases. BMC Microbiol 23, 218 (2023). https://doi.org/10.1186/s12866-023-02965-z
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DOI: https://doi.org/10.1186/s12866-023-02965-z