A virus carries a gene encoding juvenile hormone acid methyltransferase, a key regulatory enzyme in insect metamorphosis

Jun Takatsuka,Tetsuro Shinoda,Madoka Nakai

doi:10.1038/s41598-017-14059-8

Abstract

Microbial parasitism, infection, and symbiosis in animals often modulate host endocrine systems, resulting in alterations of phenotypic traits of the host that can have profound effects on the ecology and evolution of both the microorganisms and their hosts. Information about the mechanisms and genetic bases of such modulations by animal parasites is available from studies of steroid hormones. However, reports involving other hormones are scarce. We found that an insect virus, a betaentomopoxvirus, encodes a juvenile hormone acid methyltransferase that can synthesize an important insect hormone, the sesquiterpenoid juvenile hormone. Phylogenetic analysis suggested that this gene is of bacterial origin. Our study challenges the conventional view that functional enzymes in the late phase of the juvenile hormone biosynthesis pathway are almost exclusive to insects or arthropods, and shed light on juvenoid hormone synthesis beyond Eukaryota. This striking example demonstrates that even animal parasites having no metabolic pathways for molecules resembling host hormones can nevertheless influence the synthesis of such hormones, and provides a new context for studying animal parasite strategies in diverse systems such as host-parasite, host-symbiont or host-vector-parasite.

Highlights

Parasites, pathogens, and symbionts use other organisms to perpetuate themselves in nature
We report that SAM-dependent MTase encoded in the genome of a betaentomopoxvirus, Mythimna separata entomopoxvirus (MySEV), is a functional JHA methyltransferase (JHAMT), and that the viral JHAMT is likely to be descended from a member of the domain Bacteria
Our study demonstrates that MySEV possesses a functional JHAMT gene

Summary

Introduction

Pathogens, and symbionts (simplified hereafter to parasites unless otherwise mentioned) use other organisms to perpetuate themselves in nature. Parasites are likely to have evolved particular strategies to utilize their hosts for completing their life cycles and enhancing their transmission Recent work on both plant-parasite and animal-parasite interactions suggests that host endocrine systems are important targets that parasites manipulate for their reproductive success[1,2]. Striking characteristics of the pathological effects of EPV infection on the host are a prolonged larval period in the final instar and the inhibition of metamorphosis to pupae[9,10,11] (e.g., Fig. 1) These phenotypic characteristics of EPV infections may be advantageous for EPV transmission in host insect populations via increased virus production or inhibition of pupation-associated behaviour[10]. We report that SAM-dependent MTase encoded in the genome of a betaentomopoxvirus, Mythimna separata entomopoxvirus (MySEV), is a functional JHAMT, and that the viral JHAMT is likely to be descended from a member of the domain Bacteria

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