Pinewood nematode induced changes in the assembly process of gallery microbiomes benefit its vector beetle's development.

Publisher: ASM Press Country of Publication: United States NLM ID: 101634614 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2165-0497 (Electronic) Linking ISSN: 21650497 NLM ISO Abbreviation: Microbiol Spectr Subsets: MEDLINE

Original Publication: Washington, DC : ASM Press, 2013-

Coleoptera*/microbiology ; Coleoptera*/parasitology ; Microbiota* ; Plant Diseases*/microbiology ; Plant Diseases*/parasitology ; Pinus*/microbiology ; Pinus*/parasitology ; RNA, Ribosomal, 16S*/genetics; Animals ; Bacteria/classification ; Bacteria/genetics ; Bacteria/isolation & purification ; Actinobacteria/genetics ; Actinobacteria/isolation & purification ; Actinobacteria/classification ; Insect Vectors/microbiology ; Insect Vectors/parasitology ; Firmicutes/genetics ; Firmicutes/isolation & purification ; Ophiostomatales/genetics ; Ophiostomatales/physiology ; Ophiostomatales/growth & development ; Ophiostomatales/isolation & purification ; Nematoda/microbiology ; Fungi/genetics ; Fungi/classification ; Fungi/physiology

Microbiomes play crucial roles in insect adaptation, especially under stress such as pathogen invasion. Yet, how beneficial microbiomes assemble remains unclear. The wood-boring beetle Monochamus alternatus , a major pest and vector of the pine wilt disease (PWD) nematode, offers a unique model. We conducted controlled experiments using amplicon sequencing (16S rRNA and ITS) within galleries where beetles and microbes interact. PWD significantly altered bacterial and fungal communities, suggesting distinct assembly processes. Deterministic factors like priority effects, host selection, and microbial interactions shaped microbiome composition, distinguishing healthy from PWN-infected galleries. Actinobacteria, Firmicutes, and Ophiostomataceae emerged as potentially beneficial, aiding beetle's development and pathogen resistance. This study unveils how nematode-induced changes in gallery microbiomes influence beetle's development, shedding light on microbiome assembly amid insect-pathogen interactions. Insights gleaned enhance understanding of PWD spread and suggest novel management strategies via microbiome manipulation.IMPORTANCEThis study explores the assembly process of gallery microbiomes associated with a wood-boring beetles, Monochamus alternatus , a vector of the pine wilt disease (PWD). By conducting controlled comparison experiments and employing amplicon approaches, the study reveals significant changes in taxonomic composition and functional adaptation of bacterial and fungal communities induced by PWD. It identifies deterministic processes, including priority effects, host selection, and microbial interactions, as major drivers in microbiome assembly. Additionally, the study highlights the presence of potentially beneficial microbes such as Actinobacteria, Firmicutes, and Ophiostomataceae, which could enhance beetle development and resistance to pathogens. These findings shed light on the intricate interplay among insects, microbiomes, and pathogens, contributing to a deeper understanding of PWD prevalence and suggesting innovative management strategies through microbiome manipulation.
Competing Interests: The authors declare no conflict of interest.

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32070486 MOST | National Natural Science Foundation of China (NSFC); 32088102 MOST | National Natural Science Foundation of China (NSFC); 2021YFC2600100 Ministry of Science and Technology of the People's Republic of China (MOST)

Keywords: Monochamus alternatus; beneficial microbiota; gallery; microbial assembly; pinewood nematode

0 (RNA, Ribosomal, 16S)

Date Created: 20240911 Date Completed: 20241004 Latest Revision: 20241005

20241005

PMC11448173

10.1128/spectrum.01412-24

39258937