Genome of the rams horn snail Biomphalaria straminea: an obligate intermediate host of schistosomiasis

Wenyan Nong; Yifei Yu; Madeleine Emma Aase-Remedios; Yichun Xie; Wai Lok So; Yiqian Li; Cheuk Fung Wong; Toby Baril; Sean Law; Sheung Yee Lai; Jasmine Haimovitz; Thomas Swale; Shan-shan Chen; Zhen-peng Kai; Xi Sun; Zhongdao Wu; Alexander Hayward; David Ellard Keith Ferrier; Jerome Hui

doi:10.1093/gigascience/giac012

Genome of the rams horn snail Biomphalaria straminea: an obligate intermediate host of schistosomiasis

Wenyan Nong
, Yifei Yu
, Madeleine Emma Aase-Remedios
, Yichun Xie
, Wai Lok So
, Yiqian Li
, Cheuk Fung Wong
, Toby Baril
, Sean Law
, Sheung Yee Lai
, Jasmine Haimovitz
, Thomas Swale
, Shan-shan Chen
, Zhen-peng Kai
, Xi Sun
, Zhongdao Wu
, Alexander Hayward^*
, David Ellard Keith Ferrier^*
, Jerome Hui^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

Background: Schistosomiasis, or bilharzia, is a parasitic disease caused by trematode flatworms of the genus Schistosoma. Infection by Schistosoma mansoni in humans results when cercariae emerge into water from freshwater snails in the genus Biomphalaria and seek out and penetrate human skin. The snail Biomphalaria straminea is native to South America and is now also present in Central America and China, and represents a potential vector host for spreading schistosomiasis. To date, genomic information for the genus is restricted to the neotropical species Biomphalaria glabrata. This limits understanding of the biology and management of other schistosomiasis vectors, such as B. straminea.

Findings: Using a combination of Illumina short‐read, 10X Genomics linked‐read, and Hi‐C sequencing data, our 1.005 Gb B. straminea genome assembly is of high contiguity, with a scaffold N50 of 25.3 Mb. Transcriptomes from adults were also obtained. Developmental homeobox genes, hormonal genes, and stress-response genes were identified, and repeat content was annotated (40.68% of genomic content). Comparisons with other mollusc genomes (including Gastropoda, Bivalvia, and Cephalopoda) revealed syntenic conservation, patterns of homeobox gene linkage indicative of evolutionary changes to gene clusters, expansion of heat shock protein genes, and the presence of sesquiterpenoid and cholesterol metabolic pathway genes in Gastropoda. In addition, hormone treatment together with RT-qPCR assay reveal a sesquiterpenoid hormone responsive system in B. straminea, illustrating that this renowned insect hormonal system is also present in the lophotrochozoan lineage.

Conclusion: This study provides the first genome assembly for the snail B. straminea and offers an unprecedented opportunity to address a variety of phenomena related to snail vectors of schistosomiasis, as well as evolutionary and genomics questions related to molluscs more widely.

Original language	English
Article number	giac012
Number of pages	13
Journal	GigaScience
Volume	11
Early online date	15 Feb 2022
DOIs	https://doi.org/10.1093/gigascience/giac012
Publication status	E-pub ahead of print - 15 Feb 2022

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

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Copyright The Author(s) 2022. Published by Oxford University Press GigaScience. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
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Nong, W., Yu, Y., Aase-Remedios, M. E., Xie, Y., So, W. L., Li, Y., Wong, C. F., Baril, T., Law, S., Lai, S. Y., Haimovitz, J., Swale, T., Chen, S., Kai, Z., Sun, X., Wu, Z., Hayward, A., Ferrier, D. E. K., & Hui, J. (2022). Genome of the rams horn snail Biomphalaria straminea: an obligate intermediate host of schistosomiasis. GigaScience, 11, Article giac012. Advance online publication. https://doi.org/10.1093/gigascience/giac012

@article{69ac0a964a294587a7c743d2302952ae,

title = "Genome of the rams horn snail Biomphalaria straminea: an obligate intermediate host of schistosomiasis",

abstract = "Background: Schistosomiasis, or bilharzia, is a parasitic disease caused by trematode flatworms of the genus Schistosoma. Infection by Schistosoma mansoni in humans results when cercariae emerge into water from freshwater snails in the genus Biomphalaria and seek out and penetrate human skin. The snail Biomphalaria straminea is native to South America and is now also present in Central America and China, and represents a potential vector host for spreading schistosomiasis. To date, genomic information for the genus is restricted to the neotropical species Biomphalaria glabrata. This limits understanding of the biology and management of other schistosomiasis vectors, such as B. straminea. Findings: Using a combination of Illumina short‐read, 10X Genomics linked‐read, and Hi‐C sequencing data, our 1.005 Gb B. straminea genome assembly is of high contiguity, with a scaffold N50 of 25.3 Mb. Transcriptomes from adults were also obtained. Developmental homeobox genes, hormonal genes, and stress-response genes were identified, and repeat content was annotated (40.68\% of genomic content). Comparisons with other mollusc genomes (including Gastropoda, Bivalvia, and Cephalopoda) revealed syntenic conservation, patterns of homeobox gene linkage indicative of evolutionary changes to gene clusters, expansion of heat shock protein genes, and the presence of sesquiterpenoid and cholesterol metabolic pathway genes in Gastropoda. In addition, hormone treatment together with RT-qPCR assay reveal a sesquiterpenoid hormone responsive system in B. straminea, illustrating that this renowned insect hormonal system is also present in the lophotrochozoan lineage. Conclusion: This study provides the first genome assembly for the snail B. straminea and offers an unprecedented opportunity to address a variety of phenomena related to snail vectors of schistosomiasis, as well as evolutionary and genomics questions related to molluscs more widely.",

author = "Wenyan Nong and Yifei Yu and Aase-Remedios, \{Madeleine Emma\} and Yichun Xie and So, \{Wai Lok\} and Yiqian Li and Wong, \{Cheuk Fung\} and Toby Baril and Sean Law and Lai, \{Sheung Yee\} and Jasmine Haimovitz and Thomas Swale and Shan-shan Chen and Zhen-peng Kai and Xi Sun and Zhongdao Wu and Alexander Hayward and Ferrier, \{David Ellard Keith\} and Jerome Hui",

note = "This work was supported by the Hong Kong Research Grant Council Collaborative Research Fund (C4015-20EF), General Research Fund (14100919), NSFC/RGC Joint Research Scheme (N\_CUHK401/21), and The Chinese University of Hong Kong Direct Grant (4053433, 4053489). Y.Y., W.L.S., C.F.W., S.T.S.L., and Y.L. were supported by the Ph.D. studentships of The Chinese University of Hong Kong. A.H. is supported by a Biotechnology and Biological Sciences Research Council (BBSRC) David Phillips Fellowship (BB/N020146/1). T.B. is supported by a studentship from the Biotechnology and Biological Sciences Research Council-funded South West Biosciences Doctoral Training Partnership (BB/M009122/1). M.E.A.R. is supported by a Ph.D. studentship from the School of Biology and St Andrews University.",

year = "2022",

month = feb,

day = "15",

doi = "10.1093/gigascience/giac012",

language = "English",

volume = "11",

journal = "GigaScience",

issn = "2047-217X",

publisher = "Oxford University Press",

}

Nong, W, Yu, Y, Aase-Remedios, ME, Xie, Y, So, WL, Li, Y, Wong, CF, Baril, T, Law, S, Lai, SY, Haimovitz, J, Swale, T, Chen, S, Kai, Z, Sun, X, Wu, Z, Hayward, A, Ferrier, DEK & Hui, J 2022, 'Genome of the rams horn snail Biomphalaria straminea: an obligate intermediate host of schistosomiasis', GigaScience, vol. 11, giac012. https://doi.org/10.1093/gigascience/giac012

TY - JOUR

T1 - Genome of the rams horn snail Biomphalaria straminea

T2 - an obligate intermediate host of schistosomiasis

AU - Nong, Wenyan

AU - Yu, Yifei

AU - Aase-Remedios, Madeleine Emma

AU - Xie, Yichun

AU - So, Wai Lok

AU - Li, Yiqian

AU - Wong, Cheuk Fung

AU - Baril, Toby

AU - Law, Sean

AU - Lai, Sheung Yee

AU - Haimovitz, Jasmine

AU - Swale, Thomas

AU - Chen, Shan-shan

AU - Kai, Zhen-peng

AU - Sun, Xi

AU - Wu, Zhongdao

AU - Hayward, Alexander

AU - Ferrier, David Ellard Keith

AU - Hui, Jerome

N1 - This work was supported by the Hong Kong Research Grant Council Collaborative Research Fund (C4015-20EF), General Research Fund (14100919), NSFC/RGC Joint Research Scheme (N_CUHK401/21), and The Chinese University of Hong Kong Direct Grant (4053433, 4053489). Y.Y., W.L.S., C.F.W., S.T.S.L., and Y.L. were supported by the Ph.D. studentships of The Chinese University of Hong Kong. A.H. is supported by a Biotechnology and Biological Sciences Research Council (BBSRC) David Phillips Fellowship (BB/N020146/1). T.B. is supported by a studentship from the Biotechnology and Biological Sciences Research Council-funded South West Biosciences Doctoral Training Partnership (BB/M009122/1). M.E.A.R. is supported by a Ph.D. studentship from the School of Biology and St Andrews University.

PY - 2022/2/15

Y1 - 2022/2/15

N2 - Background: Schistosomiasis, or bilharzia, is a parasitic disease caused by trematode flatworms of the genus Schistosoma. Infection by Schistosoma mansoni in humans results when cercariae emerge into water from freshwater snails in the genus Biomphalaria and seek out and penetrate human skin. The snail Biomphalaria straminea is native to South America and is now also present in Central America and China, and represents a potential vector host for spreading schistosomiasis. To date, genomic information for the genus is restricted to the neotropical species Biomphalaria glabrata. This limits understanding of the biology and management of other schistosomiasis vectors, such as B. straminea. Findings: Using a combination of Illumina short‐read, 10X Genomics linked‐read, and Hi‐C sequencing data, our 1.005 Gb B. straminea genome assembly is of high contiguity, with a scaffold N50 of 25.3 Mb. Transcriptomes from adults were also obtained. Developmental homeobox genes, hormonal genes, and stress-response genes were identified, and repeat content was annotated (40.68% of genomic content). Comparisons with other mollusc genomes (including Gastropoda, Bivalvia, and Cephalopoda) revealed syntenic conservation, patterns of homeobox gene linkage indicative of evolutionary changes to gene clusters, expansion of heat shock protein genes, and the presence of sesquiterpenoid and cholesterol metabolic pathway genes in Gastropoda. In addition, hormone treatment together with RT-qPCR assay reveal a sesquiterpenoid hormone responsive system in B. straminea, illustrating that this renowned insect hormonal system is also present in the lophotrochozoan lineage. Conclusion: This study provides the first genome assembly for the snail B. straminea and offers an unprecedented opportunity to address a variety of phenomena related to snail vectors of schistosomiasis, as well as evolutionary and genomics questions related to molluscs more widely.

AB - Background: Schistosomiasis, or bilharzia, is a parasitic disease caused by trematode flatworms of the genus Schistosoma. Infection by Schistosoma mansoni in humans results when cercariae emerge into water from freshwater snails in the genus Biomphalaria and seek out and penetrate human skin. The snail Biomphalaria straminea is native to South America and is now also present in Central America and China, and represents a potential vector host for spreading schistosomiasis. To date, genomic information for the genus is restricted to the neotropical species Biomphalaria glabrata. This limits understanding of the biology and management of other schistosomiasis vectors, such as B. straminea. Findings: Using a combination of Illumina short‐read, 10X Genomics linked‐read, and Hi‐C sequencing data, our 1.005 Gb B. straminea genome assembly is of high contiguity, with a scaffold N50 of 25.3 Mb. Transcriptomes from adults were also obtained. Developmental homeobox genes, hormonal genes, and stress-response genes were identified, and repeat content was annotated (40.68% of genomic content). Comparisons with other mollusc genomes (including Gastropoda, Bivalvia, and Cephalopoda) revealed syntenic conservation, patterns of homeobox gene linkage indicative of evolutionary changes to gene clusters, expansion of heat shock protein genes, and the presence of sesquiterpenoid and cholesterol metabolic pathway genes in Gastropoda. In addition, hormone treatment together with RT-qPCR assay reveal a sesquiterpenoid hormone responsive system in B. straminea, illustrating that this renowned insect hormonal system is also present in the lophotrochozoan lineage. Conclusion: This study provides the first genome assembly for the snail B. straminea and offers an unprecedented opportunity to address a variety of phenomena related to snail vectors of schistosomiasis, as well as evolutionary and genomics questions related to molluscs more widely.

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DO - 10.1093/gigascience/giac012

M3 - Article

SN - 2047-217X

VL - 11

JO - GigaScience

JF - GigaScience

M1 - giac012

ER -

Genome of the rams horn snail Biomphalaria straminea: an obligate intermediate host of schistosomiasis

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Genome of the rams horn snail Biomphalaria straminea: an obligate intermediate host of schistosomiasis

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