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

Theodor Bilharz Research Institute

Bibliographic Information

Authors: Xu S.; Zhang Y.-W.-Q.; Habib M.R.; Li S.-Z.; Yuan Y.; Ke W.H.; Jiang N.; Dong H.; Zhao Q.-P.

Journal: Parasites and Vectors

Publisher: BioMed Central Ltd

Publication Date: 17 February 2023

Volume / Issue: Volume 16 / Issue 1

Article No.: 73

ISSN: 17563305

DOI: 10.1186/s13071-022-05642-8

Scopus: View on Scopus

PubMed: 36804043

Document Type: Article

Access: All Open Access; Gold Open Access; Green Open Access

Authors and Affiliations

Xu S., Department of Parasitology, School of Basic Medical Sciences, Wuhan University, Hubei Province, Wuhan, China; Zhang Y.-W.-Q., Department of Parasitology, School of Basic Medical Sciences, Wuhan University, Hubei Province, Wuhan, China; Habib M.R., Medical Malacology Laboratory, Theodor Bilharz Research Institute, Giza, Egypt; Li S.-Z., National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, National Center for Tropical Diseases Research, WHO Collaborating Center for Tropical Diseases, Key Laboratory of Parasite and Vector Biology, Ministry of Health, Shanghai, China; Yuan Y., Hubei Center for Disease Control and Prevention, Hubei Province, Wuhan, China; Ke W.H., Department of Parasitology, School of Basic Medical Sciences, Wuhan University, Hubei Province, Wuhan, China; Jiang N., Department of Parasitology, School of Basic Medical Sciences, Wuhan University, Hubei Province, Wuhan, China; Dong H., Department of Parasitology, School of Basic Medical Sciences, Wuhan University, Hubei Province, Wuhan, China; Zhao Q.-P., Department of Parasitology, School of Basic Medical Sciences, Wuhan University, Hubei Province, Wuhan, China

Abstract

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: [Figure not available: see fulltext.]. © 2023, The Author(s).

Keywords

Alternative oxidase; Biomphalaria glabrata; Development; Oviposition; Reproductive system; RNA interference; Animals; Biomphalaria; Female; Oxidoreductases; Schistosoma mansoni; cytochrome c; cytochrome c oxidase; double stranded RNA; enhanced green fluorescent protein; messenger RNA; oxidoreductase; adult; animal experiment; animal tissue; AOX gene; Article; controlled study; developmental stage; egg laying; egg production; gene; gene expression; gene expression profiling; gene knockdown; histology; intermediate host; male; nonhuman; protein expression; protein function; real time polymerase chain reaction; respiratory chain; RNA extraction; schistosomiasis; snail; spermatic cord; transmission electron microscopy; animal; physiology

Citation Information

Scopus Citations: 4

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