Interactive Gene Expression Between Metarhizium anisopliae JEF-290 and Longhorned Tick Haemaphysalis longicornis at Early Stage of Infection.

Mi Rong Lee,Se Jin Lee,Doo-Hyung Lee,Woo Jin Kim,Jong Cheol Kim,Jae Su Kim,So Eun Park

doi:10.3389/fphys.2021.643389

Mi Rong Lee, Se Jin Lee + Show 5 more

Open Access

https://doi.org/10.3389/fphys.2021.643389

Copy DOI

Abstract

The longhorned tick, Haemaphysalis longicornis (Acari: Ixodidae), is a hard tick and a vector for severe fever with thrombocytopenia syndrome (SFTS) virus. The number of patients infected with SFTS is rapidly increasing. Recently, the invertebrate pathogen Metarhizium anisopliae JEF-290 was reported to be useful to control the tick as an alternative to chemical acaricides, which are not easily applicable in human living areas where the tick is widely spread. In this study, we analyzed how the tick and the fungal pathogen interact at the transcriptional level. Field-collected tick nymphs were treated with JEF-290 conidia at 1 × 108 conidia/ml. In the early stage of infection with 2.5% mortality, the infected ticks were subjected to RNA sequencing, and non-infected ticks and fungal masses served as controls. Fungus and tick genes were mostly up-regulated at the early stage of infection. In the gene set enrichment analysis of the infecting fungus, catabolic processes that included lipids, phospholipids, and detoxification processes, the response to oxidative stress, and toxic substances were significantly up-regulated. In this fungal up-regulation, various lipase, antioxidant enzyme, and hydrolase genes were highly transcribed. The gene set enrichment analysis of the infected tick showed that many peptide synthesis processes including translation, peptide metabolism, ribonucleotide metabolism, and energy production processes that included ATP generation and ADP metabolism were significantly up-regulated. Structurally, mitochondria and ribosome subunit genes in ticks were highly transcribed to upregulate these processes. Together these results indicate that JEF-290 initiates process that infects the tick while the tick actively defends against the fungal attack. This work provides background to improve our understanding of the early stage of fungal infection in longhorned tick.

Highlights

Haemaphysalis longicornis (Acari: Ixodidae), the longhorned tick is an important vector for human disease, and known to transmit severe fever with thrombocytopenia syndrome virus (SFTSV), Rickettsia japonica, and Coxiella burnetii (Mahara, 1997)
As a result of whole genome sequencing of M. anisopliae JEF290, a total of 11,868,389,082 bases were identified with N50 of 26,851 bp (Supplementary Table 1)
Comparison of the orthologs of the six different genus of entomopathogenic fungi revealed that all strains shared 5,320 genes, and JEF290, M. robertstii, M. riley, and M. acridum shared 698 genes (Supplementary Figure 1)

Summary

Introduction

Haemaphysalis longicornis (Acari: Ixodidae), the longhorned tick is an important vector for human disease, and known to transmit severe fever with thrombocytopenia syndrome virus (SFTSV), Rickettsia japonica, and Coxiella burnetii (Mahara, 1997). SFTSV causes vomiting, diarrhea, high fever, and thrombocytopenia, and the mortality ranges from 2% to as high as 30% (Gai et al, 2012). The longhorned tick is an important pest for livestock such as deer, sheep, and cattle. In New Zealand and Australia, the tick can reduce cattle production by 25% (Heath, 2016). This tick mediates cattle diseases from Theileria species, which are threats to the livestock industry (Hammer et al, 2015)

Methods

Results

Conclusion