Characterization of Venom and Oviduct Components of Parasitoid Wasp Asobara japonica.

During natural parasitization, Asobara japonica wasps introduce lateral oviduct (LO) components into their Drosophila hosts soon after the venom injection to neutralize its strong toxicity; otherwise, the host will die. Although the orchestrated relationship between the venom and LO components neces...

Full description

Bibliographic Details
Main Authors: Shunsuke Furihata, Takashi Matsumura, Makiko Hirata, Tetsuya Mizutani, Noriyo Nagata, Michiyo Kataoka, Yukie Katayama, Tsutomu Omatsu, Hitoshi Matsumoto, Yoichi Hayakawa
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4965004?pdf=render
_version_ 1819042098122326016
author Shunsuke Furihata
Takashi Matsumura
Makiko Hirata
Tetsuya Mizutani
Noriyo Nagata
Michiyo Kataoka
Yukie Katayama
Tsutomu Omatsu
Hitoshi Matsumoto
Yoichi Hayakawa
author_facet Shunsuke Furihata
Takashi Matsumura
Makiko Hirata
Tetsuya Mizutani
Noriyo Nagata
Michiyo Kataoka
Yukie Katayama
Tsutomu Omatsu
Hitoshi Matsumoto
Yoichi Hayakawa
author_sort Shunsuke Furihata
collection DOAJ
description During natural parasitization, Asobara japonica wasps introduce lateral oviduct (LO) components into their Drosophila hosts soon after the venom injection to neutralize its strong toxicity; otherwise, the host will die. Although the orchestrated relationship between the venom and LO components necessary for successful parasitism has attracted the attention of many researchers in this field, the molecular natures of both factors remain ambiguous. We here showed that precipitation of the venom components by ultracentrifugation yielded a toxic fraction that was inactivated by ultraviolet light irradiation, boiling, and sonication, suggesting that it is a virus-like entity. Morphological observation of the precipitate after ultracentrifugation showed small spherical heterogeneous virus-like particles 20-40 nm in diameter. The venom's detrimental effect on D. melanogaster larvae was not directly neutralized by the LO components but blocked by a hemolymphal neutralizing factor activated by the LO factor. Furthermore, we found that A. japonica venom and LO components acted similarly on the larvae of the common cutworm Spodoptera litura: the venom injection caused mortality but coinjection of the LO factor protected S. litura larvae from the venom's toxicity. In contrast, D. ficusphila and D. bipectinata, which are closely related to D. melanogaster but non-habitual host species of A. japonica, were not negatively affected by A. japonica venom due to an intrinsic neutralizing activity in their hemolymph, indicating that these species must have acquired a neutralizer of A. japonica venom during evolution. These results give new insights into the characteristics of both the venom and LO components: A. japonica females have utilized the virus-like toxic venom factor to exploit a wider range of host species after the evolutionary process enabled them to use the LO factor for activation of the host hemolymph neutralizer precursor, although the non-habitual host Drosophila species possess an active intrinsic neutralizer in their hemolymph.
first_indexed 2024-12-21T09:35:29Z
format Article
id doaj.art-fde27c5212164f01b3abedc375dcd526
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-21T09:35:29Z
publishDate 2016-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-fde27c5212164f01b3abedc375dcd5262022-12-21T19:08:39ZengPublic Library of Science (PLoS)PLoS ONE1932-62032016-01-01117e016021010.1371/journal.pone.0160210Characterization of Venom and Oviduct Components of Parasitoid Wasp Asobara japonica.Shunsuke FurihataTakashi MatsumuraMakiko HirataTetsuya MizutaniNoriyo NagataMichiyo KataokaYukie KatayamaTsutomu OmatsuHitoshi MatsumotoYoichi HayakawaDuring natural parasitization, Asobara japonica wasps introduce lateral oviduct (LO) components into their Drosophila hosts soon after the venom injection to neutralize its strong toxicity; otherwise, the host will die. Although the orchestrated relationship between the venom and LO components necessary for successful parasitism has attracted the attention of many researchers in this field, the molecular natures of both factors remain ambiguous. We here showed that precipitation of the venom components by ultracentrifugation yielded a toxic fraction that was inactivated by ultraviolet light irradiation, boiling, and sonication, suggesting that it is a virus-like entity. Morphological observation of the precipitate after ultracentrifugation showed small spherical heterogeneous virus-like particles 20-40 nm in diameter. The venom's detrimental effect on D. melanogaster larvae was not directly neutralized by the LO components but blocked by a hemolymphal neutralizing factor activated by the LO factor. Furthermore, we found that A. japonica venom and LO components acted similarly on the larvae of the common cutworm Spodoptera litura: the venom injection caused mortality but coinjection of the LO factor protected S. litura larvae from the venom's toxicity. In contrast, D. ficusphila and D. bipectinata, which are closely related to D. melanogaster but non-habitual host species of A. japonica, were not negatively affected by A. japonica venom due to an intrinsic neutralizing activity in their hemolymph, indicating that these species must have acquired a neutralizer of A. japonica venom during evolution. These results give new insights into the characteristics of both the venom and LO components: A. japonica females have utilized the virus-like toxic venom factor to exploit a wider range of host species after the evolutionary process enabled them to use the LO factor for activation of the host hemolymph neutralizer precursor, although the non-habitual host Drosophila species possess an active intrinsic neutralizer in their hemolymph.http://europepmc.org/articles/PMC4965004?pdf=render
spellingShingle Shunsuke Furihata
Takashi Matsumura
Makiko Hirata
Tetsuya Mizutani
Noriyo Nagata
Michiyo Kataoka
Yukie Katayama
Tsutomu Omatsu
Hitoshi Matsumoto
Yoichi Hayakawa
Characterization of Venom and Oviduct Components of Parasitoid Wasp Asobara japonica.
PLoS ONE
title Characterization of Venom and Oviduct Components of Parasitoid Wasp Asobara japonica.
title_full Characterization of Venom and Oviduct Components of Parasitoid Wasp Asobara japonica.
title_fullStr Characterization of Venom and Oviduct Components of Parasitoid Wasp Asobara japonica.
title_full_unstemmed Characterization of Venom and Oviduct Components of Parasitoid Wasp Asobara japonica.
title_short Characterization of Venom and Oviduct Components of Parasitoid Wasp Asobara japonica.
title_sort characterization of venom and oviduct components of parasitoid wasp asobara japonica
url http://europepmc.org/articles/PMC4965004?pdf=render
work_keys_str_mv AT shunsukefurihata characterizationofvenomandoviductcomponentsofparasitoidwaspasobarajaponica
AT takashimatsumura characterizationofvenomandoviductcomponentsofparasitoidwaspasobarajaponica
AT makikohirata characterizationofvenomandoviductcomponentsofparasitoidwaspasobarajaponica
AT tetsuyamizutani characterizationofvenomandoviductcomponentsofparasitoidwaspasobarajaponica
AT noriyonagata characterizationofvenomandoviductcomponentsofparasitoidwaspasobarajaponica
AT michiyokataoka characterizationofvenomandoviductcomponentsofparasitoidwaspasobarajaponica
AT yukiekatayama characterizationofvenomandoviductcomponentsofparasitoidwaspasobarajaponica
AT tsutomuomatsu characterizationofvenomandoviductcomponentsofparasitoidwaspasobarajaponica
AT hitoshimatsumoto characterizationofvenomandoviductcomponentsofparasitoidwaspasobarajaponica
AT yoichihayakawa characterizationofvenomandoviductcomponentsofparasitoidwaspasobarajaponica