Molecular Characterization of Rotifers and Their Potential Use in the Biological Control of Biomphalaria

BackgroundSchistosomiasis is one of the most important tropical parasitic diseases worldwide. Biomphalaria straminea, the intermediate host of Schistosoma mansoni, has invaded and spread to Southern China since 1974 and may pose enormous threats to public health. Controlling intermediate host snails...

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Main Authors: Datao Lin, Suoyu Xiang, Benjamin Sanogo, Yousheng Liang, Xi Sun, Zhongdao Wu
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2021.744352/full
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author Datao Lin
Datao Lin
Suoyu Xiang
Suoyu Xiang
Benjamin Sanogo
Benjamin Sanogo
Yousheng Liang
Xi Sun
Xi Sun
Zhongdao Wu
Zhongdao Wu
author_facet Datao Lin
Datao Lin
Suoyu Xiang
Suoyu Xiang
Benjamin Sanogo
Benjamin Sanogo
Yousheng Liang
Xi Sun
Xi Sun
Zhongdao Wu
Zhongdao Wu
author_sort Datao Lin
collection DOAJ
description BackgroundSchistosomiasis is one of the most important tropical parasitic diseases worldwide. Biomphalaria straminea, the intermediate host of Schistosoma mansoni, has invaded and spread to Southern China since 1974 and may pose enormous threats to public health. Controlling intermediate host snails is an effective strategy in schistosomiasis intervention. However, the only effective chemical molluscicide, niclosamide, currently recommended by WHO may cause environmental pollution, loss of biodiversity, and high costs. Thus, to counter intermediate hosts, a sustainable and environmentally friendly tool is urgently needed. Here, we conducted field investigations to collect and identify a potential snail competitor rotifer and evaluated its molluscicide effect.ResultsIn this study, we collected two samples of rotifers from Shenzhen. We found both red and black phenotypic B. straminea snails at the sampling sites. We identified the rotifer population as a species of the genus Philodina according to the amplification and phylogenetic analysis results of coxI gene. We found that rotifer exposure did not significantly affect the hatching rate of B. straminea eggs but promoted the killing of juvenile snails. Meanwhile, rotifer exposure did not significantly alter the fecundity of B. straminea quantified by the number of eggs per egg mass, the number of egg masses per snail, and the number of eggs per snail; but the snails exposed to rotifers showed lower fecundity performance than the control snails. Importantly, rotifer exposure could significantly affect the development of juvenile B. straminea, showing a smaller shell diameter of the exposed snails than that of the control snails. In addition, rotifer exposure affected the life span of B. straminea snails, showing a 16.61% decline in the average life span. After rotifer exposure, the S. mansoni-infected B. straminea snails died significantly faster than those without rotifer exposure. Similar findings were observed in S. mansoni-infected Biomphalaria glabrata snails. These results implied that rotifer exposure significantly promoted the mortality of S. mansoni-infected B. straminea and B. glabrata.ConclusionsOur study demonstrated the potential molluscicide effect of rotifers on intermediate hosts under laboratory conditions. Our findings may provide new insights into the development of biocontrol strategies for snail-borne disease transmission.
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spelling doaj.art-d86cbfcadb8e4a7e9d60168e7fb529002022-12-21T21:29:55ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882021-09-011110.3389/fcimb.2021.744352744352Molecular Characterization of Rotifers and Their Potential Use in the Biological Control of BiomphalariaDatao Lin0Datao Lin1Suoyu Xiang2Suoyu Xiang3Benjamin Sanogo4Benjamin Sanogo5Yousheng Liang6Xi Sun7Xi Sun8Zhongdao Wu9Zhongdao Wu10Department of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou, ChinaProvincial Engineering Technology Research Center for Diseases-Vectors Control, Key Laboratory of Tropical Disease Control, Ministry of Education, Guangzhou, ChinaDepartment of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou, ChinaProvincial Engineering Technology Research Center for Diseases-Vectors Control, Key Laboratory of Tropical Disease Control, Ministry of Education, Guangzhou, ChinaDepartment of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou, ChinaProvincial Engineering Technology Research Center for Diseases-Vectors Control, Key Laboratory of Tropical Disease Control, Ministry of Education, Guangzhou, ChinaJiangsu Provincial Key Laboratory on Parasite and Vector Control Technology, Jiangsu Institute of Parasitic Diseases, Wuxi, ChinaDepartment of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou, ChinaProvincial Engineering Technology Research Center for Diseases-Vectors Control, Key Laboratory of Tropical Disease Control, Ministry of Education, Guangzhou, ChinaDepartment of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, Guangzhou, ChinaProvincial Engineering Technology Research Center for Diseases-Vectors Control, Key Laboratory of Tropical Disease Control, Ministry of Education, Guangzhou, ChinaBackgroundSchistosomiasis is one of the most important tropical parasitic diseases worldwide. Biomphalaria straminea, the intermediate host of Schistosoma mansoni, has invaded and spread to Southern China since 1974 and may pose enormous threats to public health. Controlling intermediate host snails is an effective strategy in schistosomiasis intervention. However, the only effective chemical molluscicide, niclosamide, currently recommended by WHO may cause environmental pollution, loss of biodiversity, and high costs. Thus, to counter intermediate hosts, a sustainable and environmentally friendly tool is urgently needed. Here, we conducted field investigations to collect and identify a potential snail competitor rotifer and evaluated its molluscicide effect.ResultsIn this study, we collected two samples of rotifers from Shenzhen. We found both red and black phenotypic B. straminea snails at the sampling sites. We identified the rotifer population as a species of the genus Philodina according to the amplification and phylogenetic analysis results of coxI gene. We found that rotifer exposure did not significantly affect the hatching rate of B. straminea eggs but promoted the killing of juvenile snails. Meanwhile, rotifer exposure did not significantly alter the fecundity of B. straminea quantified by the number of eggs per egg mass, the number of egg masses per snail, and the number of eggs per snail; but the snails exposed to rotifers showed lower fecundity performance than the control snails. Importantly, rotifer exposure could significantly affect the development of juvenile B. straminea, showing a smaller shell diameter of the exposed snails than that of the control snails. In addition, rotifer exposure affected the life span of B. straminea snails, showing a 16.61% decline in the average life span. After rotifer exposure, the S. mansoni-infected B. straminea snails died significantly faster than those without rotifer exposure. Similar findings were observed in S. mansoni-infected Biomphalaria glabrata snails. These results implied that rotifer exposure significantly promoted the mortality of S. mansoni-infected B. straminea and B. glabrata.ConclusionsOur study demonstrated the potential molluscicide effect of rotifers on intermediate hosts under laboratory conditions. Our findings may provide new insights into the development of biocontrol strategies for snail-borne disease transmission.https://www.frontiersin.org/articles/10.3389/fcimb.2021.744352/fullBiomphalaria stramineaBiomphalaria glabrataSchistosoma mansonirotiferPhilodinabiocontrol strategy
spellingShingle Datao Lin
Datao Lin
Suoyu Xiang
Suoyu Xiang
Benjamin Sanogo
Benjamin Sanogo
Yousheng Liang
Xi Sun
Xi Sun
Zhongdao Wu
Zhongdao Wu
Molecular Characterization of Rotifers and Their Potential Use in the Biological Control of Biomphalaria
Frontiers in Cellular and Infection Microbiology
Biomphalaria straminea
Biomphalaria glabrata
Schistosoma mansoni
rotifer
Philodina
biocontrol strategy
title Molecular Characterization of Rotifers and Their Potential Use in the Biological Control of Biomphalaria
title_full Molecular Characterization of Rotifers and Their Potential Use in the Biological Control of Biomphalaria
title_fullStr Molecular Characterization of Rotifers and Their Potential Use in the Biological Control of Biomphalaria
title_full_unstemmed Molecular Characterization of Rotifers and Their Potential Use in the Biological Control of Biomphalaria
title_short Molecular Characterization of Rotifers and Their Potential Use in the Biological Control of Biomphalaria
title_sort molecular characterization of rotifers and their potential use in the biological control of biomphalaria
topic Biomphalaria straminea
Biomphalaria glabrata
Schistosoma mansoni
rotifer
Philodina
biocontrol strategy
url https://www.frontiersin.org/articles/10.3389/fcimb.2021.744352/full
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