Parasitization of <i>Aphis gossypii</i> Glover by <i>Binodoxys communis</i> Gahan Causes Shifts in the Ovarian Bacterial Microbiota

Background: <i>Aphis gossypii</i> Glover is an important agricultural pest distributed worldwide. <i>Binodoxys communis</i> Gahan is the main parasitoid wasp of <i>A. gossypii</i>. Previous studies have shown that parasitization causes reduced egg production in &l...

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Main Authors: Jinming Li, Zhe An, Junyu Luo, Xiangzhen Zhu, Li Wang, Kaixin Zhang, Dongyang Li, Jichao Ji, Lin Niu, Xueke Gao, Jinjie Cui
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/14/4/314
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author Jinming Li
Zhe An
Junyu Luo
Xiangzhen Zhu
Li Wang
Kaixin Zhang
Dongyang Li
Jichao Ji
Lin Niu
Xueke Gao
Jinjie Cui
author_facet Jinming Li
Zhe An
Junyu Luo
Xiangzhen Zhu
Li Wang
Kaixin Zhang
Dongyang Li
Jichao Ji
Lin Niu
Xueke Gao
Jinjie Cui
author_sort Jinming Li
collection DOAJ
description Background: <i>Aphis gossypii</i> Glover is an important agricultural pest distributed worldwide. <i>Binodoxys communis</i> Gahan is the main parasitoid wasp of <i>A. gossypii</i>. Previous studies have shown that parasitization causes reduced egg production in <i>A. gossypii</i>, but the effects of parasitism on the symbiotic bacteria in the host ovaries are unknown. Results: In this study, we analyzed the microbial communities in the ovaries of <i>A. gossypii</i> without and after parasitization. Whether parasitized or not, <i>Buchnera</i> was the dominant genus of symbiotic bacteria in the ovaries, followed by facultative symbionts including <i>Arsenophonus</i>, <i>Pseudomonas</i>, and <i>Acinetobacter</i>. The relative abundance of <i>Buchnera</i> in the aphid ovary increased after parasitization for 1 d in both third-instar nymph and adult stages, but decreased after parasitization for 3 d. The shifts in the relative abundance of <i>Arsenophonus</i> in both stages were the same as those observed for <i>Buchnera.</i> In addition, the relative abundance of <i>Serratia</i> remarkably decreased after parasitization for 1 d and increased after parasitization for 3 d. A functional predictive analysis of the control and parasitized ovary microbiomes revealed that pathways primarily enriched in parasitization were “amino acid transport and metabolism” and “energy production and conversion.” Finally, RT-qPCR analysis was performed on <i>Buchnera</i>, <i>Arsenophonus</i>, and <i>Serratia</i>. The results of RT-qPCR were the same as the results of 16S rDNA sequencing. Conclusions: These results provide a framework for investigating shifts in the microbial communities in host ovaries, which may be responsible for reduced egg production in aphids. These findings also broaden our understanding of the interactions among aphids, parasitoid wasps, and endosymbionts.
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spelling doaj.art-38391df6ca164b22b1153dac1e3b536d2023-11-17T19:45:48ZengMDPI AGInsects2075-44502023-03-0114431410.3390/insects14040314Parasitization of <i>Aphis gossypii</i> Glover by <i>Binodoxys communis</i> Gahan Causes Shifts in the Ovarian Bacterial MicrobiotaJinming Li0Zhe An1Junyu Luo2Xiangzhen Zhu3Li Wang4Kaixin Zhang5Dongyang Li6Jichao Ji7Lin Niu8Xueke Gao9Jinjie Cui10Zhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, ChinaZhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, ChinaZhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, ChinaZhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, ChinaZhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, ChinaZhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, ChinaZhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, ChinaZhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, ChinaZhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, ChinaZhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, ChinaZhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, ChinaBackground: <i>Aphis gossypii</i> Glover is an important agricultural pest distributed worldwide. <i>Binodoxys communis</i> Gahan is the main parasitoid wasp of <i>A. gossypii</i>. Previous studies have shown that parasitization causes reduced egg production in <i>A. gossypii</i>, but the effects of parasitism on the symbiotic bacteria in the host ovaries are unknown. Results: In this study, we analyzed the microbial communities in the ovaries of <i>A. gossypii</i> without and after parasitization. Whether parasitized or not, <i>Buchnera</i> was the dominant genus of symbiotic bacteria in the ovaries, followed by facultative symbionts including <i>Arsenophonus</i>, <i>Pseudomonas</i>, and <i>Acinetobacter</i>. The relative abundance of <i>Buchnera</i> in the aphid ovary increased after parasitization for 1 d in both third-instar nymph and adult stages, but decreased after parasitization for 3 d. The shifts in the relative abundance of <i>Arsenophonus</i> in both stages were the same as those observed for <i>Buchnera.</i> In addition, the relative abundance of <i>Serratia</i> remarkably decreased after parasitization for 1 d and increased after parasitization for 3 d. A functional predictive analysis of the control and parasitized ovary microbiomes revealed that pathways primarily enriched in parasitization were “amino acid transport and metabolism” and “energy production and conversion.” Finally, RT-qPCR analysis was performed on <i>Buchnera</i>, <i>Arsenophonus</i>, and <i>Serratia</i>. The results of RT-qPCR were the same as the results of 16S rDNA sequencing. Conclusions: These results provide a framework for investigating shifts in the microbial communities in host ovaries, which may be responsible for reduced egg production in aphids. These findings also broaden our understanding of the interactions among aphids, parasitoid wasps, and endosymbionts.https://www.mdpi.com/2075-4450/14/4/314parasitoids<i>Buchnera</i><i>Serratia</i><i>Arsenophonus</i>host–parasite interactionsaphid
spellingShingle Jinming Li
Zhe An
Junyu Luo
Xiangzhen Zhu
Li Wang
Kaixin Zhang
Dongyang Li
Jichao Ji
Lin Niu
Xueke Gao
Jinjie Cui
Parasitization of <i>Aphis gossypii</i> Glover by <i>Binodoxys communis</i> Gahan Causes Shifts in the Ovarian Bacterial Microbiota
Insects
parasitoids
<i>Buchnera</i>
<i>Serratia</i>
<i>Arsenophonus</i>
host–parasite interactions
aphid
title Parasitization of <i>Aphis gossypii</i> Glover by <i>Binodoxys communis</i> Gahan Causes Shifts in the Ovarian Bacterial Microbiota
title_full Parasitization of <i>Aphis gossypii</i> Glover by <i>Binodoxys communis</i> Gahan Causes Shifts in the Ovarian Bacterial Microbiota
title_fullStr Parasitization of <i>Aphis gossypii</i> Glover by <i>Binodoxys communis</i> Gahan Causes Shifts in the Ovarian Bacterial Microbiota
title_full_unstemmed Parasitization of <i>Aphis gossypii</i> Glover by <i>Binodoxys communis</i> Gahan Causes Shifts in the Ovarian Bacterial Microbiota
title_short Parasitization of <i>Aphis gossypii</i> Glover by <i>Binodoxys communis</i> Gahan Causes Shifts in the Ovarian Bacterial Microbiota
title_sort parasitization of i aphis gossypii i glover by i binodoxys communis i gahan causes shifts in the ovarian bacterial microbiota
topic parasitoids
<i>Buchnera</i>
<i>Serratia</i>
<i>Arsenophonus</i>
host–parasite interactions
aphid
url https://www.mdpi.com/2075-4450/14/4/314
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