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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...

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Autores principales: Furihata, Shunsuke, Matsumura, Takashi, Hirata, Makiko, Mizutani, Tetsuya, Nagata, Noriyo, Kataoka, Michiyo, Katayama, Yukie, Omatsu, Tsutomu, Matsumoto, Hitoshi, Hayakawa, Yoichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4965004/
https://www.ncbi.nlm.nih.gov/pubmed/27467595
http://dx.doi.org/10.1371/journal.pone.0160210
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author Furihata, Shunsuke
Matsumura, Takashi
Hirata, Makiko
Mizutani, Tetsuya
Nagata, Noriyo
Kataoka, Michiyo
Katayama, Yukie
Omatsu, Tsutomu
Matsumoto, Hitoshi
Hayakawa, Yoichi
author_facet Furihata, Shunsuke
Matsumura, Takashi
Hirata, Makiko
Mizutani, Tetsuya
Nagata, Noriyo
Kataoka, Michiyo
Katayama, Yukie
Omatsu, Tsutomu
Matsumoto, Hitoshi
Hayakawa, Yoichi
author_sort Furihata, Shunsuke
collection PubMed
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.
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spelling pubmed-49650042016-08-18 Characterization of Venom and Oviduct Components of Parasitoid Wasp Asobara japonica Furihata, Shunsuke Matsumura, Takashi Hirata, Makiko Mizutani, Tetsuya Nagata, Noriyo Kataoka, Michiyo Katayama, Yukie Omatsu, Tsutomu Matsumoto, Hitoshi Hayakawa, Yoichi PLoS One Research Article 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. Public Library of Science 2016-07-28 /pmc/articles/PMC4965004/ /pubmed/27467595 http://dx.doi.org/10.1371/journal.pone.0160210 Text en © 2016 Furihata et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Furihata, Shunsuke
Matsumura, Takashi
Hirata, Makiko
Mizutani, Tetsuya
Nagata, Noriyo
Kataoka, Michiyo
Katayama, Yukie
Omatsu, Tsutomu
Matsumoto, Hitoshi
Hayakawa, Yoichi
Characterization of Venom and Oviduct Components of Parasitoid Wasp Asobara japonica
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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4965004/
https://www.ncbi.nlm.nih.gov/pubmed/27467595
http://dx.doi.org/10.1371/journal.pone.0160210
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