Root rot destabilizes the Sanqi rhizosphere core fungal microbiome by reducing the negative connectivity of beneficial microbes

Author:

Wang Baoying1,Geng Yuhang1,Lin Yulan1,Xia Qing1,Wei Fugang2,Yang Shaozhou2,Huang Xinqi134ORCID,Zhang Jinbo135,Cai Zucong1345,Zhao Jun134ORCID

Affiliation:

1. School of Geography, Nanjing Normal University, Nanjing, China

2. Miaoxiang Sanqi Technology Co., Ltd., Wenshan, China

3. Jiangsu Engineering Research Center for Soil Utilization & Sustainable Agriculture, Nanjing, China

4. Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and Application, Nanjing, China

5. Key Laboratory of Virtual Geographical Environment (Nanjing Normal University), Ministry of Education, Nanjing, China

Abstract

ABSTRACT The stability of microbial communities, especially among core taxa, is essential for supporting plant health. However, the impacts of disease infection on the stability of rhizosphere fungal core microbiome remain largely unexplored. In this study, we delved into the effects of root rot infestation on the community structure, function, network complexity, and stability of Sanqi fungal core microbiomes, employing amplicon sequencing combined with co-occurrence network and cohesion analyses. Our investigation revealed that root rot disease led to a decrease in the α-diversity but an increase in the β-diversity of the Sanqi fungal core microbiomes in the rhizosphere. Notably, Ilyonectria , Plectosphaerella, and Fusarium emerged as indicator species in the rhizosphere core microbiome of root rot-infected Sanqi plants, while Mortierella predominated as the dominant biomarker taxa in healthy soils. Additionally, root rot diminished the complexity and modularity of the rhizosphere networks by reducing the metrics associated with nodes, edges, degrees, and modularity. Furthermore, root rot resulted in a reduction in the proportion of negative connections in the network and the negative/positive cohesion of the entire core fungal microbiome. Particularly noteworthy was the observation that root rot infection destabilized the rhizosphere core fungal microbiome by weakening the negative connectivity associated with beneficial agents. Collectively, these results highlight the significance of the negative connectivity of beneficial agents in ensuring the stability of core microbial community. IMPORTANCE Root rot disease has been reported as the most devastating disease in the production process of artificial cultivated Sanqi ginseng, which seriously threatens the Sanqi industry. This study provides valuable insights into how root rot influences microbial relationships within the community. These findings open up opportunities for disease prevention and the promotion of plant health by regulating microbial interactions. In summary, the research sheds light on the ecological consequences of root rot on rhizosphere fungal microbiomes and offers potential strategies for managing soil-borne diseases and enhancing plant health.

Funder

MOST | National Natural Science Foundation of China

Yunnan Province Expert Workstation Construction Project

Jiangsu Funding Program for Excellent Postdoctoral Talent

Publisher

American Society for Microbiology

Subject

Ecology,Applied Microbiology and Biotechnology,Food Science,Biotechnology

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