Bacterial community and genome analysis of cytoplasmic incompatibility-inducing Wolbachia in American serpentine leafminer, Liriomyza trifolii

Ajeng K Pramono; Ardhiani K Hidayanti; Yohsuke Tagami; Hiroki Ando

doi:10.3389/fmicb.2024.1304401

Bacterial community and genome analysis of cytoplasmic incompatibility-inducing Wolbachia in American serpentine leafminer, Liriomyza trifolii

Front Microbiol. 2024 Feb 6:15:1304401. doi: 10.3389/fmicb.2024.1304401. eCollection 2024.

Authors

Ajeng K Pramono¹, Ardhiani K Hidayanti^{2

3}, Yohsuke Tagami⁴, Hiroki Ando^{1

5}

Affiliations

¹ Laboratory of Phage Biologics, Graduate School of Medicine, Gifu University, Gifu, Japan.
² School of Biological Environment, The United Graduate School of Agricultural Science, Gifu University, Gifu, Japan.
³ School of Life Sciences and Technology, Institut Teknologi Bandung (ITB), Bandung, Indonesia.
⁴ Laboratory of Applied Entomology, Faculty of Agriculture, Shizuoka University, Shizuoka, Japan.
⁵ Center for One Medicine Innovative Translational Research (COMIT), Gifu University, Gifu, Japan.

Abstract

Liriomyza trifolii, an agricultural pest, is occasionally infected by Wolbachia. A Wolbachia strain present in Liriomyza trifolii is associated with cytoplasmic incompatibility (CI) effects, leading to the death of embryos resulting from incompatible crosses between antibiotic-treated or naturally Wolbachia-free strain females and Wolbachia-infected males. In this study, high-throughput sequencing of hypervariable rRNA genes was employed to characterize the bacterial community in Wolbachia-infected L. trifolii without antibiotic treatment. The analysis revealed that Wolbachia dominates the bacterial community in L. trifolii, with minor presence of Acinetobacter, Pseudomonas, and Limnobacter. To elucidate the genetic basis of the CI phenotype, metagenomic sequencing was also conducted to assemble the genome of the Wolbachia strain. The draft-genome of the Wolbachia strain wLtri was 1.35 Mbp with 34% GC content and contained 1,487 predicted genes. Notably, within the wLtri genome, there are three distinct types of cytoplasmic incompatibility factor (cif) genes: Type I, Type III, and Type V cifA;B. These genes are likely responsible for inducing the strong cytoplasmic incompatibility observed in L. trifolii.

Keywords: CIF; Liriomyza trifolii; Wolbachia; cytoplasmic incompatibility factor; phage WO.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was partly funded by a grant from the Japan Society for the Promotion of Science (JSPS) KAKENHI to HA (Grant Numbers: 20H03723, 15K21770) and YT (Grant Number: JP419K06069).