Microbial changes and associated metabolic responses modify host plant adaptation in Stephanitis nashi

• Published in: Insect science 2024-12, Vol.31 (6), p.1789-1809
• Main Authors: Li, Tong‐Pu, Wang, Chen‐Hao, Xie, Jia‐Chu, Wang, Meng‐Ke, Chen, Jie, Zhu, Yu‐Xi, Hao, De‐Jun, Hong, Xiao‐Yue
• Format: Article
• Language: English
• Subjects: Adaptability; Adaptation; Adaptation, Physiological; Animals; Bacteria; Bacteria - metabolism; Correlation analysis; Fruit trees; Fruits; Fungi; Fungi - physiology; Hemiptera - microbiology; Hemiptera - physiology; Herbivory; Heteroptera - microbiology; Heteroptera - physiology; host plant adaptation; Host plants; insect–microbe interaction; Kinases; Metabolic pathways; Metabolic response; Metabolism; metabolite; Metabolites; microbiome; Microbiomes; Microbiota; Microorganisms; Pests; Physiological effects; Plant layout; Signal transduction; Stephanitis; Stephanitis nashi; Symbiosis
• ISSN: 1672-9609; 1744-7917
• DOI: 10.1111/1744-7917.13340

Symbiotic microorganisms are essential for the physiological processes of herbivorous pests, including the pear lace bug Stephanitis nashi, which is known for causing extensive damage to garden plants and fruit trees due to its exceptional adaptability to diverse host plants. However, the specific functional effects of the microbiome on the adaptation of S. nashi to its host plants remains unclear. Here, we identified significant microbial changes in S. nashi on 2 different host plants, crabapple and cherry blossom, characterized by the differences in fungal diversity as well as bacterial and fungal community structures, with abundant correlations between bacteria or fungi. Consistent with the microbiome changes, S. nashi that fed on cherry blossom demonstrated decreased metabolites and downregulated key metabolic pathways, such as the arginine and mitogen‐activated protein kinase signaling pathway, which were crucial for host plant adaptation. Furthermore, correlation analysis unveiled numerous correlations between differential microorganisms and differential metabolites, which were influenced by the interactions between bacteria or fungi. These differential bacteria, fungi, and associated metabolites may modify the key metabolic pathways in S. nashi, aiding its adaptation to different host plants. These results provide valuable insights into the alteration in microbiome and function of S. nashi adapted to different host plants, contributing to a better understanding of pest invasion and dispersal from a microbial perspective. This study demonstrated changes in microbial diversity and the reshaping of microbial community structure in the pear lace bug Stephanitis nashi when it fed on 2 different host plants, and showed how S. nashi mobilized a series of metabolic reactions to adapt to these host plants. Association analysis further clarified the one‐to‐one correspondence between differential bacteria, differential fungi, and functional responses in this process, which revealed the mechanisms of S. nashi adaptation to 2 different host plants from a microbiological perspective.