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Inhibition of alternative oxidase disrupts the development and oviposition of Biomphalaria glabrata snails

BACKGROUND: Biomphalaria glabrata is one of the main intermediate hosts of Schistosoma mansoni, the most widespread species of Schistosoma. Our previous studies proved that alternative oxidase (AOX), the terminal oxidase in the mitochondrial respiratory chain, widely exists in several species of int...

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Autores principales: Xu, Sha, Zhang, Yang-Wen-Qing, Habib, Mohamed R., Li, Shi-Zhu, Yuan, Yi, Ke, Wei Hao, Jiang, Ni, Dong, Huifen, Zhao, Qin-Ping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9938623/
https://www.ncbi.nlm.nih.gov/pubmed/36804043
http://dx.doi.org/10.1186/s13071-022-05642-8
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author Xu, Sha
Zhang, Yang-Wen-Qing
Habib, Mohamed R.
Li, Shi-Zhu
Yuan, Yi
Ke, Wei Hao
Jiang, Ni
Dong, Huifen
Zhao, Qin-Ping
author_facet Xu, Sha
Zhang, Yang-Wen-Qing
Habib, Mohamed R.
Li, Shi-Zhu
Yuan, Yi
Ke, Wei Hao
Jiang, Ni
Dong, Huifen
Zhao, Qin-Ping
author_sort Xu, Sha
collection PubMed
description BACKGROUND: Biomphalaria glabrata is one of the main intermediate hosts of Schistosoma mansoni, the most widespread species of Schistosoma. Our previous studies proved that alternative oxidase (AOX), the terminal oxidase in the mitochondrial respiratory chain, widely exists in several species of intermediate host snails of Schistosoma. Meanwhile, inhibition of AOX activity in Oncomelania hupensis snails could dramatically enhance the molluscicidal effect of niclosamide. As a hermaphroditic aquatic mollusc, the high fecundity and population density of B. glabrata increase the difficulty of snail control, which is one of the critical strategies for schistosomiasis elimination. The present study aimed to investigate the possible role of AOX in the development and fecundity of B. glabrata snail, which could be manipulated more manageable than other species of intermediate host snails of Schistosoma. METHODS: The dynamic expression of the AOX gene was investigated in different developmental stages and tissues of B. glabrata, with morphological change and oviposition behaviour observed from juvenile to adult snails. Furtherly, dsRNA-mediated knockdown of BgAOX mRNA and the AOX protein activity inhibiting was performed to investigate the effect of AOX on the development and oviposition of snails. RESULTS: The BgAOX gene expression profile is highly related to the development from late juveniles to adults, especially to the reproductive system of snails, with a positive correlation of 0.975 between egg production and BgAOX relative expression in ovotestis of snails. The inhibition of BgAOX at the transcriptional level and AOX activity could efficiently inhibit snail growth. However, the interference at the BgAOX protein activity level led to more severe tissue damage and more significant inhibition of oviposition than at the transcriptional level. This inhibition of growth and oviposition decreased gradually with the increase in the snail size. CONCLUSIONS: The inhibition of AOX could efficiently disrupt the development and oviposition of B. glabrata snails, and the intervention targeting AOX at the juvenile stage is more effective for snails. This investigation explored the role of AOX in the growth and development of snails. It would benefit snail control in the future by providing a potential target while using molluscicides more efficiently. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05642-8.
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spelling pubmed-99386232023-02-19 Inhibition of alternative oxidase disrupts the development and oviposition of Biomphalaria glabrata snails Xu, Sha Zhang, Yang-Wen-Qing Habib, Mohamed R. Li, Shi-Zhu Yuan, Yi Ke, Wei Hao Jiang, Ni Dong, Huifen Zhao, Qin-Ping Parasit Vectors Research BACKGROUND: Biomphalaria glabrata is one of the main intermediate hosts of Schistosoma mansoni, the most widespread species of Schistosoma. Our previous studies proved that alternative oxidase (AOX), the terminal oxidase in the mitochondrial respiratory chain, widely exists in several species of intermediate host snails of Schistosoma. Meanwhile, inhibition of AOX activity in Oncomelania hupensis snails could dramatically enhance the molluscicidal effect of niclosamide. As a hermaphroditic aquatic mollusc, the high fecundity and population density of B. glabrata increase the difficulty of snail control, which is one of the critical strategies for schistosomiasis elimination. The present study aimed to investigate the possible role of AOX in the development and fecundity of B. glabrata snail, which could be manipulated more manageable than other species of intermediate host snails of Schistosoma. METHODS: The dynamic expression of the AOX gene was investigated in different developmental stages and tissues of B. glabrata, with morphological change and oviposition behaviour observed from juvenile to adult snails. Furtherly, dsRNA-mediated knockdown of BgAOX mRNA and the AOX protein activity inhibiting was performed to investigate the effect of AOX on the development and oviposition of snails. RESULTS: The BgAOX gene expression profile is highly related to the development from late juveniles to adults, especially to the reproductive system of snails, with a positive correlation of 0.975 between egg production and BgAOX relative expression in ovotestis of snails. The inhibition of BgAOX at the transcriptional level and AOX activity could efficiently inhibit snail growth. However, the interference at the BgAOX protein activity level led to more severe tissue damage and more significant inhibition of oviposition than at the transcriptional level. This inhibition of growth and oviposition decreased gradually with the increase in the snail size. CONCLUSIONS: The inhibition of AOX could efficiently disrupt the development and oviposition of B. glabrata snails, and the intervention targeting AOX at the juvenile stage is more effective for snails. This investigation explored the role of AOX in the growth and development of snails. It would benefit snail control in the future by providing a potential target while using molluscicides more efficiently. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05642-8. BioMed Central 2023-02-17 /pmc/articles/PMC9938623/ /pubmed/36804043 http://dx.doi.org/10.1186/s13071-022-05642-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Xu, Sha
Zhang, Yang-Wen-Qing
Habib, Mohamed R.
Li, Shi-Zhu
Yuan, Yi
Ke, Wei Hao
Jiang, Ni
Dong, Huifen
Zhao, Qin-Ping
Inhibition of alternative oxidase disrupts the development and oviposition of Biomphalaria glabrata snails
title Inhibition of alternative oxidase disrupts the development and oviposition of Biomphalaria glabrata snails
title_full Inhibition of alternative oxidase disrupts the development and oviposition of Biomphalaria glabrata snails
title_fullStr Inhibition of alternative oxidase disrupts the development and oviposition of Biomphalaria glabrata snails
title_full_unstemmed Inhibition of alternative oxidase disrupts the development and oviposition of Biomphalaria glabrata snails
title_short Inhibition of alternative oxidase disrupts the development and oviposition of Biomphalaria glabrata snails
title_sort inhibition of alternative oxidase disrupts the development and oviposition of biomphalaria glabrata snails
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9938623/
https://www.ncbi.nlm.nih.gov/pubmed/36804043
http://dx.doi.org/10.1186/s13071-022-05642-8
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