Whole genome analysis of a schistosomiasis-transmitting freshwater snail

doi:10.1038/ncomms15451

. 2017 May 16:8:15451.

doi: 10.1038/ncomms15451.

Whole genome analysis of a schistosomiasis-transmitting freshwater snail

Coen M Adema¹, LaDeana W Hillier², Catherine S Jones³, Eric S Loker¹, Matty Knight^{4

5}, Patrick Minx², Guilherme Oliveira^{6

7}, Nithya Raghavan, Andrew Shedlock⁸, Laurence Rodrigues do Amaral⁹, Halime D Arican-Goktas¹⁰, Juliana G Assis⁶, Elio Hideo Baba⁶, Olga L Baron¹¹, Christopher J Bayne¹², Utibe Bickham-Wright¹³, Kyle K Biggar¹⁴, Michael Blouin¹², Bryony C Bonning¹⁵, Chris Botka¹⁶, Joanna M Bridger¹⁰, Katherine M Buckley¹⁷, Sarah K Buddenborg¹, Roberta Lima Caldeira¹⁸, Julia Carleton¹⁹, Omar S Carvalho¹⁸, Maria G Castillo²⁰, Iain W Chalmers²¹, Mikkel Christensens²², Sandra Clifton², Celine Cosseau²³, Christine Coustau¹¹, Richard M Cripps²⁴, Yesid Cuesta-Astroz⁶, Scott F Cummins²⁵, Leon di Stephano^{26

27}, Nathalie Dinguirard¹³, David Duval²³, Scott Emrich²⁸, Cédric Feschotte¹⁹, Rene Feyereisen²⁹, Peter FitzGerald³⁰, Catrina Fronick², Lucinda Fulton², Richard Galinier²³, Sandra G Gava⁶, Michael Geusz³¹, Kathrin K Geyer²¹, Gloria I Giraldo-Calderón²⁸, Matheus de Souza Gomes⁹, Michelle A Gordy³¹, Benjamin Gourbal²³, Christoph Grunau²³, Patrick C Hanington³², Karl F Hoffmann²¹, Daniel Hughes²², Judith Humphries³³, Daniel J Jackson³⁴, Liana K Jannotti-Passos⁶, Wander de Jesus Jeremias⁶, Susan Jobling³⁵, Bishoy Kamel³⁶, Aurélie Kapusta¹⁹, Satwant Kaur³⁵, Joris M Koene³⁷, Andrea B Kohn³⁸, Dan Lawson²², Scott P Lawton³⁹, Di Liang²⁵, Yanin Limpanont²⁵, Sijun Liu¹⁵, Anne E Lockyer³⁵, TyAnna L Lovato²⁴, Fernanda Ludolf⁶, Vince Magrini², Donald P McManus⁴⁰, Monica Medina³⁶, Milind Misra¹, Guillaume Mitta²³, Gerald M Mkoji⁴¹, Michael J Montague⁴², Cesar Montelongo²⁰, Leonid L Moroz³⁸, Monica C Munoz-Torres⁴³, Umar Niazi²¹, Leslie R Noble³, Francislon S Oliveira⁶, Fabiano S Pais⁶, Anthony T Papenfuss^{26

27}, Rob Peace⁴⁴, Janeth J Pena¹, Emmanuel A Pila³², Titouan Quelais²³, Brian J Raney⁴⁵, Jonathan P Rast¹⁷, David Rollinson⁴⁶, Izinara C Rosse⁶, Bronwyn Rotgans²⁵, Edwin J Routledge³⁵, Kathryn M Ryan²⁴, Larissa L S Scholte⁶, Kenneth B Storey¹⁴, Martin Swain²¹, Jacob A Tennessen¹², Chad Tomlinson², Damian L Trujillo²⁴, Emanuela V Volpi⁴⁷, Anthony J Walker³⁹, Tianfang Wang²⁵, Ittiprasert Wannaporn⁴, Wesley C Warren², Xiao-Jun Wu¹³, Timothy P Yoshino¹³, Mohammed Yusuf^{48

49}, Si-Ming Zhang¹, Min Zhao²⁵, Richard K Wilson²

Affiliations

¹ Center for Theoretical and Evolutionary Immunology, Biology, University of New Mexico, Albuquerque New Mexico 87131 USA.
² The McDonnell Genome Institute, Washington University, Saint Louis, Missouri 63108 USA.
³ Institute of Biological and Environmental Sciences, School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK.
⁴ Department of Microbiology, Immunology &Tropical Medicine and Research Center for Neglected Diseases of Poverty, School of Medicine &Health Sciences, The George Washington University, Washington, DC 20037, USA.
⁵ Division of Science &Mathematics, University of the District of Columbia, 4200 Connecticut Avenue NW Washington, Washington DC 20008, USA.
⁶ René Rachou Research Center, FIOCRUZ-Minas, Belo Horizonte, MG Brazil.
⁷ Vale Institute of Technology, Belém, Brazil.
⁸ College of Charleston, Biology Department, Medical University of South Carolina College of Graduate Studies Hollings Marine Laboratory Charleston, Charleston, South Carolina 29412 USA.
⁹ Laboratory of Bioinformatics and Molecular Analysis, Institute of Genetics and Biochemistry Federal University of Uberlândia - Campus Patos de Minas (UFU), CEP 38700-128 Patos de Minas, Brasil.
¹⁰ Department of Life Sciences, College of Health and Life Sciences, Brunel University, London, Uxbridge UB8 3PH, UK.
¹¹ Institut Sophia Agrobiotech, INRA/CNRS/UNS, Sophia Antipolis, France.
¹² Department of Integrative Biology, Oregon State University, 3029 Cordley Hall, Corvallis, Oregon 97331 USA.
¹³ Department of Pathobiological Sciences, University of Wisconsin - School of Veterinary Medicine, 2015 Linden Dr Madison, Wisconsin 53706 USA.
¹⁴ Institute of Biochemisty and Department of Biology, Carleton University, Ottawa Ontario, Canada.
¹⁵ Iowa State University, Ames, Iowa 50011 USA.
¹⁶ Department of Information Technology, Harvard Medical School, 107 Avenue Louis Pasteur, Boston, Massachusetts 02115 USA.
¹⁷ Sunnybrook Health Sciences Centre, Department of Immunology, University of Toronto, 2075 Bayview Avenue, Rm. S126, Toronto, Ontario M4N 3M5, Canada.
¹⁸ Laboratorio de Helmintologia e Malacologia Médica, FIOCRUZ-Minas, René Rachou Research Center, Belo Horizonte, Brazil.
¹⁹ Department of Human Genetics. University of Utah. 15 North 2030 East, Salt Lake City, Utah 84112, USA.
²⁰ Biology, New Mexico State University, Las Cruces, New Mexico 88003, USA.
²¹ Animal and Microbial Sciences Research Theme, IBERS, Aberystwyth University, Aberystwyth SY23 3FG, UK.
²² EMBL-EBI, Wellcome Genome Campus, CB10 1, UK.
²³ Univ. Perpignan Via Domitia, IHPE UMR 5244, CNRS, IFREMER, Univ. Montpellier, F-66860 Perpignan, France.
²⁴ Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131, USA.
²⁵ Faculty of Science, Health and Education, University of the Sunshine Coast, Maroochydore, Queensland 4558, Australia.
²⁶ The Walter and Eliza Hall Institute for Medical Research 1G Royal Parade, Parkville, Victoria 3052 Australia.
²⁷ Bioinformatics and Cancer Genomics lab Lorenzo and Pamela Galli, Melanoma Research Fellow Peter MacCallum Cancer Centre St Andrews Place, East Melbourne, Victoria 3002, Australia.
²⁸ Genomics and Bioinformatics Core Facility, 19 Galvin Life Sciences, University of Notre Dame, Notre Dame, Indiana 46556 USA.
²⁹ University of Copenhagen, Faculty of Science, Department of Plant and Environmental Sciences, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark.
³⁰ Genome Analysis Unit, National Cancer Institute, National Institutes of Health, Bethesda, Maryland 20892, USA.
³¹ Biological Sciences, Bowling Green State University, Bowling Green, Ohio 43403 USA.
³² Department of Public Health Sciences, University of Alberta, 3-57F South Academic Building, Edmonton, Alberta T6G 1C9, Canada.
³³ Department of Biology, Lawrence University, Appleton Wisconsin 54911 USA.
³⁴ Courant Research Centre Geobiology, Georg-August University of Göttingen, Goldschmidtstraße 3, 37077 Göttingen, Germany.
³⁵ Institute of Environment, Health &Societies, Environment and Health Theme, Brunel University London, Uxbridge UB8 3PH, UK.
³⁶ Department of Biology, Pennsylvania State University, University Park, Pennsylvania 16802 USA.
³⁷ Faculteit der Aard- en Levenswetenschappen, Vrije Universiteit, De Boelelaan 1085-1087 1081 HV Amsterdam, The Netherlands.
³⁸ The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd, St Augustine, Florida 32080, USA.
³⁹ Molecular Parasitology Laboratory, School of Life Sciences Pharmacy and Chemistry, Kingston University, Kingston upon Thames, Surrey KT1 2EE. UK.
⁴⁰ Molecular Parasitology Laboratory, QIMR Berghofer Medical Research Institute, Brisbane, Queensland 4006, Australia.
⁴¹ Kenya Medical Research Institute. P.O. Box 54840, 00200. Nairobi, Kenya.
⁴² Department of Neuroscience, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania 19104 USA.
⁴³ Berkeley Bioinformatics Open-Source Projects, Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, One Cyclotron Road MS 977, Berkeley, California, 94720, USA.
⁴⁴ Department of Systems and Computer Engineering, Carleton University, Ottawa Ontario, Canada.
⁴⁵ Genomics Institute, UC Santa Cruz, UC Santa Cruz, Santa Cruz, California 95064, USA.
⁴⁶ Parasites and Vectors Division, London Centre for Neglected Tropical Disease Research, Wolfson Wellcome Biomedical Laboratories, Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK.
⁴⁷ Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, 115 New Cavendish Street, London W1W 6UW, UK.
⁴⁸ London Centre for Nanotechnology,University College London, Gower Street, London WC1E 6BT, UK.
⁴⁹ Research Complex at Harwell, Rutherford Appleton Laboratory, Oxfordshire OX11 0FA, UK.

PMID: 28508897
PMCID: PMC5440852
DOI: 10.1038/ncomms15451

Free PMC article

Whole genome analysis of a schistosomiasis-transmitting freshwater snail

Coen M Adema et al. Nat Commun. 2017.

Free PMC article

. 2017 May 16:8:15451.

doi: 10.1038/ncomms15451.

Authors

Affiliations

¹ Center for Theoretical and Evolutionary Immunology, Biology, University of New Mexico, Albuquerque New Mexico 87131 USA.
² The McDonnell Genome Institute, Washington University, Saint Louis, Missouri 63108 USA.
³ Institute of Biological and Environmental Sciences, School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK.
⁴ Department of Microbiology, Immunology &Tropical Medicine and Research Center for Neglected Diseases of Poverty, School of Medicine &Health Sciences, The George Washington University, Washington, DC 20037, USA.
⁵ Division of Science &Mathematics, University of the District of Columbia, 4200 Connecticut Avenue NW Washington, Washington DC 20008, USA.
⁶ René Rachou Research Center, FIOCRUZ-Minas, Belo Horizonte, MG Brazil.
⁷ Vale Institute of Technology, Belém, Brazil.
⁸ College of Charleston, Biology Department, Medical University of South Carolina College of Graduate Studies Hollings Marine Laboratory Charleston, Charleston, South Carolina 29412 USA.
⁹ Laboratory of Bioinformatics and Molecular Analysis, Institute of Genetics and Biochemistry Federal University of Uberlândia - Campus Patos de Minas (UFU), CEP 38700-128 Patos de Minas, Brasil.
¹⁰ Department of Life Sciences, College of Health and Life Sciences, Brunel University, London, Uxbridge UB8 3PH, UK.
¹¹ Institut Sophia Agrobiotech, INRA/CNRS/UNS, Sophia Antipolis, France.
¹² Department of Integrative Biology, Oregon State University, 3029 Cordley Hall, Corvallis, Oregon 97331 USA.
¹³ Department of Pathobiological Sciences, University of Wisconsin - School of Veterinary Medicine, 2015 Linden Dr Madison, Wisconsin 53706 USA.
¹⁴ Institute of Biochemisty and Department of Biology, Carleton University, Ottawa Ontario, Canada.
¹⁵ Iowa State University, Ames, Iowa 50011 USA.
¹⁶ Department of Information Technology, Harvard Medical School, 107 Avenue Louis Pasteur, Boston, Massachusetts 02115 USA.
¹⁷ Sunnybrook Health Sciences Centre, Department of Immunology, University of Toronto, 2075 Bayview Avenue, Rm. S126, Toronto, Ontario M4N 3M5, Canada.
¹⁸ Laboratorio de Helmintologia e Malacologia Médica, FIOCRUZ-Minas, René Rachou Research Center, Belo Horizonte, Brazil.
¹⁹ Department of Human Genetics. University of Utah. 15 North 2030 East, Salt Lake City, Utah 84112, USA.
²⁰ Biology, New Mexico State University, Las Cruces, New Mexico 88003, USA.
²¹ Animal and Microbial Sciences Research Theme, IBERS, Aberystwyth University, Aberystwyth SY23 3FG, UK.
²² EMBL-EBI, Wellcome Genome Campus, CB10 1, UK.
²³ Univ. Perpignan Via Domitia, IHPE UMR 5244, CNRS, IFREMER, Univ. Montpellier, F-66860 Perpignan, France.
²⁴ Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131, USA.
²⁵ Faculty of Science, Health and Education, University of the Sunshine Coast, Maroochydore, Queensland 4558, Australia.
²⁶ The Walter and Eliza Hall Institute for Medical Research 1G Royal Parade, Parkville, Victoria 3052 Australia.
²⁷ Bioinformatics and Cancer Genomics lab Lorenzo and Pamela Galli, Melanoma Research Fellow Peter MacCallum Cancer Centre St Andrews Place, East Melbourne, Victoria 3002, Australia.
²⁸ Genomics and Bioinformatics Core Facility, 19 Galvin Life Sciences, University of Notre Dame, Notre Dame, Indiana 46556 USA.
²⁹ University of Copenhagen, Faculty of Science, Department of Plant and Environmental Sciences, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark.
³⁰ Genome Analysis Unit, National Cancer Institute, National Institutes of Health, Bethesda, Maryland 20892, USA.
³¹ Biological Sciences, Bowling Green State University, Bowling Green, Ohio 43403 USA.
³² Department of Public Health Sciences, University of Alberta, 3-57F South Academic Building, Edmonton, Alberta T6G 1C9, Canada.
³³ Department of Biology, Lawrence University, Appleton Wisconsin 54911 USA.
³⁴ Courant Research Centre Geobiology, Georg-August University of Göttingen, Goldschmidtstraße 3, 37077 Göttingen, Germany.
³⁵ Institute of Environment, Health &Societies, Environment and Health Theme, Brunel University London, Uxbridge UB8 3PH, UK.
³⁶ Department of Biology, Pennsylvania State University, University Park, Pennsylvania 16802 USA.
³⁷ Faculteit der Aard- en Levenswetenschappen, Vrije Universiteit, De Boelelaan 1085-1087 1081 HV Amsterdam, The Netherlands.
³⁸ The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd, St Augustine, Florida 32080, USA.
³⁹ Molecular Parasitology Laboratory, School of Life Sciences Pharmacy and Chemistry, Kingston University, Kingston upon Thames, Surrey KT1 2EE. UK.
⁴⁰ Molecular Parasitology Laboratory, QIMR Berghofer Medical Research Institute, Brisbane, Queensland 4006, Australia.
⁴¹ Kenya Medical Research Institute. P.O. Box 54840, 00200. Nairobi, Kenya.
⁴² Department of Neuroscience, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania 19104 USA.
⁴³ Berkeley Bioinformatics Open-Source Projects, Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, One Cyclotron Road MS 977, Berkeley, California, 94720, USA.
⁴⁴ Department of Systems and Computer Engineering, Carleton University, Ottawa Ontario, Canada.
⁴⁵ Genomics Institute, UC Santa Cruz, UC Santa Cruz, Santa Cruz, California 95064, USA.
⁴⁶ Parasites and Vectors Division, London Centre for Neglected Tropical Disease Research, Wolfson Wellcome Biomedical Laboratories, Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK.
⁴⁷ Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, 115 New Cavendish Street, London W1W 6UW, UK.
⁴⁸ London Centre for Nanotechnology,University College London, Gower Street, London WC1E 6BT, UK.
⁴⁹ Research Complex at Harwell, Rutherford Appleton Laboratory, Oxfordshire OX11 0FA, UK.

PMID: 28508897
PMCID: PMC5440852
DOI: 10.1038/ncomms15451

Erratum in

Corrigendum: Whole genome analysis of a schistosomiasis-transmitting freshwater snail.
Adema CM, Hillier LW, Jones CS, Loker ES, Knight M, Minx P, Oliveira G, Raghavan N, Shedlock A, do Amaral LR, Arican-Goktas HD, Assis JG, Baba EH, Baron OL, Bayne CJ, Bickham-Wright U, Biggar KK, Blouin M, Bonning BC, Botka C, Bridger JM, Buckley KM, Buddenborg SK, Lima Caldeira R, Carleton J, Carvalho OS, Castillo MG, Chalmers IW, Christensens M, Clifton S, Cosseau C, Coustau C, Cripps RM, Cuesta-Astroz Y, Cummins SF, Di Stefano L, Dinguirard N, Duval D, Emrich S, Feschotte C, Feyereisen R, FitzGerald P, Fronick C, Fulton L, Galinier R, Gava SG, Geusz M, Geyer KK, Giraldo-Calderón GI, de Souza Gomes M, Gordy MA, Gourbal B, Grunau C, Hanington PC, Hoffmann KF, Hughes D, Humphries J, Jackson DJ, Jannotti-Passos LK, de Jesus Jeremias W, Jobling S, Kamel B, Kapusta A, Kaur S, Koene JM, Kohn AB, Lawson D, Lawton SP, Liang D, Limpanont Y, Liu S, Lockyer AE, Lovato TAL, Ludolf F, Magrini V, McManus DP, Medina M, Misra M, Mitta G, Mkoji GM, Montague MJ, Montelongo C, Moroz LL, Munoz-Torres MC, Niazi U, Noble LR, Oliveira FS, Pais FS, Papenfuss AT, Peace R, Pena JJ, Pila EA, Quelais T, Raney BJ, Rast JP, Rollinson D, Rosse IC, Rotgans B, Routledge EJ, Ryan KM, Scholte LLS, Storey KB, Swai… See abstract for full author list ➔ Adema CM, et al. Nat Commun. 2017 Aug 23;8:16153. doi: 10.1038/ncomms16153. Nat Commun. 2017. PMID: 28832025 Free PMC article.

Abstract

Biomphalaria snails are instrumental in transmission of the human blood fluke Schistosoma mansoni. With the World Health Organization's goal to eliminate schistosomiasis as a global health problem by 2025, there is now renewed emphasis on snail control. Here, we characterize the genome of Biomphalaria glabrata, a lophotrochozoan protostome, and provide timely and important information on snail biology. We describe aspects of phero-perception, stress responses, immune function and regulation of gene expression that support the persistence of B. glabrata in the field and may define this species as a suitable snail host for S. mansoni. We identify several potential targets for developing novel control measures aimed at reducing snail-mediated transmission of schistosomiasis.

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Conflict of interest statement

The authors declare no competing financial interests.

Figures

**Figure 1. Candidate chemosensory receptors of B. *glabrata*.**
(a) LGUN_random_Scaffold39 contains fourteen candidate chemosensory receptor (CR) genes (BgCRa-n). Most encode seven-transmembrane domain G-protein-coupled receptor-like proteins, BgCRm and BgCRn are truncated to six-transmembrane domains. See Supplementary Data 11 for gene model identifiers. (b) Phylogenetic analysis (neighbour joining, scale bar represents amino-acid substitutions per site) of chemosensory receptors on LGUN_random_Scaffold39 (protein-level). (c) Schematic of receptor showing conserved and invariable amino acids, transmembrane domains I-VII; and location of glycosylation sites. (d) Scanning electron micrograph showing anterior tentacle, with cilia covering the surface. Scale bar, 20 μm (top); 10 μm (bottom). (e) RT–PCR gel showing amplicon for BgCR509a and actin from B. *glabrata* tentacle. (f,g) *In situ* hybridization showing sense (negative control) and antisense localization of BgCR509a mRNA in anterior tentacle section (purple). Scale bar (f): 100 μm; (g) 50 μm.

**Figure 2. TLR genes in B. *glabrata*.**
(a) Analysis of the (complete) TIR domains from BgTLRs identified seven classes (neighbour-joining tree, scale bar represents amino-acid substitutions per site). Bootstrap values shown for 1,000 replicates. Comparisons included TLRs from A. *californica* (Ac), L. *gigantea* (Lg), *Mytilus galloprovincialis* (Mg) and *C. gigas* (Cg). The presence or absence of orthologues of each class in each molluscan species is indicated. A representative of the *B. glabrata* class 1/2/3 clade is present within *A. californica*, but is independent of the *B. glabrata* TLR classes (indicated by the large pink box). Grey font indicates pseudogenes or partial genes. (b) *B. glabrata* has both single cysteine cluster (scc; blue line)- and multiple cysteine cluster (mcc; orange line) TLRs. Domain structures are shown for BgTLR classes. BgTLRs consist of an LRRNT (orange hexagon), a series of LRRs (ovals), a variable region (curvy line), LRRCT (yellow box), and transmembrane domain, and an intracellular TIR domain (hexagon). The dark blue ovals indicate well defined LRRs (predicted by LRRfinder57); light blue ovals are less confident predictions. Each of the two class 7 BgTLRs has a distinct ectodomain structure. The numbers of complete, pseudogenes (Ψ) and partial genes are indicated for each class.

**Figure 3. Expression of cardiac genes and actin genes in *B. glabrata* tissues.**
(a) Cardiac regulatory genes. (b) Cardiac structural genes. (c) Relative expression of actin genes in B. *glabrata* tissues. For (a–c), the score represents gene level aggregate of normalized FPKM counts for *de novo* assembled tissue transcripts, relative to expression levels in the heart/APO sample. The counts were scaled (with median read count as 0) to indicate expression intensity with red indicating highest, blue lowest. AG, Albumen gland; BUC, buccal mass; CNS, central nervous system; DG, digestive gland; FOOT, headfoot; HAPO, heart/APO; KID, kidney; MAN, mantle edge; OVO, ovotestes; SAL, salivary glands; STO, stomach; TRG, terminal genitalia. (d) Maximum Likelihood tree (Phylogeny.fr, scale bar represents amino-acid substitutions per site) showing phylogenetic relationships of actin genes, based on amino-acid sequence alignment (ClustalW). *Biomphalaria* -snail; *Crassostrea gigas*—oyster; *Haliotis iris*– abalone;, *Hirudo medicinalis* – leech (all lophotrochozoans); *Amphimedon queenslandica*, sponge, Prebilateria, ophotrochozoans), *Drosophila melanogaster*—fruit fly, Ecdysozoa), and the deuterostomes *Ciona intestinalis*, sea squirt; *Homo sapiens*, human. See Supplementary Note 31 for accession numbers.

**Figure 4. Comparison of molluscan shell forming proteomes.**
Circos diagram of 177 mantle-specific, secreted *Biomphalaria* gene products compared against shell forming proteomes of six other molluscs (BLASTp threshold ≤10e⁻⁶). Protein pairs that share sequence similarity in the top quartile are linked in purple, the second quartile is linked in blue, third quartile has orange links and lowest quartile of similarity has grey links. Species that occupy marine habitats are surrounded by a solid line, A finely dashed line identifies the terrestrial species *Cepea nemoralis*, the freshwater species *B. glabrata* has a coarse line. Percentages (and proportions in brackets) indicate the number of proteins that shared similarity with a *Biomphalaria* shell forming candidate gene. The width of each sector line around the ideogram is proportional to the length of that gene in basepairs. Photographs taken by DJ Jackson, with exception of photograph of *C. gigas*, by David Monniaux, distributed under a CC-A SA 3.0 license.

**Figure 5. Transposable element (TE) landscape of B. *glabrata*.**
(a) Left: proportion (%) of the genome assembly annotated as TE (black). Right: TE composition by class (indicating % of the genome corresponding to each class). (b) Evolutionary view of TE landscape. For each class, cumulative amounts of DNA (in Mb) are shown as function of the percentage of divergence from the consensus (by bins of 1%, first one being ≥0 and <1; see Supplementary Note 32 for Methods). Percentage of divergence from consensus is used as a proxy for age: the older the invasion of the TE is, the more copies will have accumulated mutations (higher percentage of divergence, right of the graph; left of the graph: youngest elements showing little divergence from consensus). Note that the result of this analysis of assembled sequence does not exclude the likelihood that intact transposable elements are present in *B. glabrata.* Colors are as in a. RC, rolling circle.

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References

1. Paraense W. L. The schistosome vectors in the Americas. Mem. Inst. Oswaldo Cruz 96, (Suppl): 7–16 (2001). - PubMed
1. King C. H. Parasites and poverty: The case of schistosomiasis. Acta Trop. 113, 95–104 (2010). - PMC - PubMed
1. Doenhoff M. J. et al.. Praziquantel: Its use in control of schistosomiasis in sub-Saharan Africa and current research needs. Parasitology 136, 1825–1835 (2009). - PubMed
1. Melman S. D. et al.. Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Negl. Trop. Dis. 3, e504–e504 (2009). - PMC - PubMed
1. Rollinson D. et al.. Time to set the agenda for schistosomiasis elimination. Acta Trop. 128, 423–440 (2013). - PubMed

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[1] Paraense W. L. The schistosome vectors in the Americas. Mem. Inst. Oswaldo Cruz 96, (Suppl): 7–16 (2001). - PubMed

[2] Paraense W. L. The schistosome vectors in the Americas. Mem. Inst. Oswaldo Cruz 96, (Suppl): 7–16 (2001). - PubMed

[3] King C. H. Parasites and poverty: The case of schistosomiasis. Acta Trop. 113, 95–104 (2010). - PMC - PubMed

[4] King C. H. Parasites and poverty: The case of schistosomiasis. Acta Trop. 113, 95–104 (2010). - PMC - PubMed

[5] Doenhoff M. J. et al.. Praziquantel: Its use in control of schistosomiasis in sub-Saharan Africa and current research needs. Parasitology 136, 1825–1835 (2009). - PubMed

[6] Doenhoff M. J. et al.. Praziquantel: Its use in control of schistosomiasis in sub-Saharan Africa and current research needs. Parasitology 136, 1825–1835 (2009). - PubMed

[7] Melman S. D. et al.. Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Negl. Trop. Dis. 3, e504–e504 (2009). - PMC - PubMed

[8] Melman S. D. et al.. Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Negl. Trop. Dis. 3, e504–e504 (2009). - PMC - PubMed

[9] Rollinson D. et al.. Time to set the agenda for schistosomiasis elimination. Acta Trop. 128, 423–440 (2013). - PubMed

[10] Rollinson D. et al.. Time to set the agenda for schistosomiasis elimination. Acta Trop. 128, 423–440 (2013). - PubMed

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Whole genome analysis of a schistosomiasis-transmitting freshwater snail

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Whole genome analysis of a schistosomiasis-transmitting freshwater snail

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