Parasitoid Jewel Wasp Mounts Multipronged Neurochemical Attack to Hijack a Host Brain.

Ryan Arvidson,Christopher Dail,Songqin Pan,Jean-Paul Urenda,Jason E Stajich,Haroun Mohammed,Cebrina Nolan,Maayan Kaiser,Frederic Libersat,Sang Soo Lee,Michael E Adams

doi:10.1074/mcp.ra118.000908

Abstract

The parasitoid emerald jewel wasp Ampulex compressa induces a compliant state of hypokinesia in its host, the American cockroach Periplaneta americana through direct envenomation of the central nervous system (CNS). To elucidate the biochemical strategy underlying venom-induced hypokinesia, we subjected the venom apparatus and milked venom to RNAseq and proteomics analyses to construct a comprehensive "venome," consisting of 264 proteins. Abundant in the venome are enzymes endogenous to the host brain, including M13 family metalloproteases, phospholipases, adenosine deaminase, hyaluronidase, and neuropeptide precursors. The amphipathic, alpha-helical ampulexins are among the most abundant venom components. Also prominent are members of the Toll/NF-κB signaling pathway, including proteases Persephone, Snake, Easter, and the Toll receptor ligand Spätzle. We find evidence that venom components are processed following envenomation. The acidic (pH∼4) venom contains unprocessed neuropeptide tachykinin and corazonin precursors and is conspicuously devoid of the corresponding processed, biologically active peptides. Neutralization of venom leads to appearance of mature tachykinin and corazonin, suggesting that the wasp employs precursors as a prolonged time-release strategy within the host brain post-envenomation. Injection of fully processed tachykinin into host cephalic ganglia elicits short-term hypokinesia. Ion channel modifiers and cytolytic toxins are absent in A. compressa venom, which appears to hijack control of the host brain by introducing a "storm" of its own neurochemicals. Our findings deepen understanding of the chemical warfare underlying host-parasitoid interactions and in particular neuromodulatory mechanisms that enable manipulation of host behavior to suit the nutritional needs of opportunistic parasitoid progeny.

Highlights

The parasitoid jewel wasp Ampulex compressa (Aculeata: Ampulicidae) injects venom directly into the central nervous system of its host, the American cockroach (Periplaneta americana) to induce a week-long lethargic state known as hypokinesia[1]
The venom apparatus is composed of two components: venom gland and venom sac (Figure 1B)
Ducts emanating from venom gland and venom sac converge at the ductus venatus, or venom duct, which projects into the stinger[48,49]

Summary

Introduction

The parasitoid jewel wasp Ampulex compressa (Aculeata: Ampulicidae) injects venom directly into the central nervous system of its host, the American cockroach (Periplaneta americana) to induce a week-long lethargic state known as hypokinesia[1]. Upon first encountering its victim, the wasp promptly and aggressively attacks, first stinging into the prothoracic ganglion to cause a 2 to 3-minute flaccid paralysis of the prothoracic legs[2]. This facilitates subsequent, precise stings into two cephalic ganglia: the brain - the central complex1 - and the subesophageal ganglion (SEG). Upon completion of stings into cephalic ganglia, the cockroach engages in vigorous grooming behavior for ~20 minutes while the wasp readies its burrow[3]. Once the stung cockroach is led into the burrow, the wasp deposits a single egg on the femur of a host leg. The venom appears to modulate descending signals from cephalic ganglia, resulting in suppression of host escape behavior, without affecting other behaviors[6]

Results

Discussion

Conclusion