Whole genome analysis of a schistosomiasis-transmitting freshwater snail

Coen M Adema, LaDeana W Hillier, Catherine S Jones, Eric S Loker, Matty Knight, Patrick Minx, Guilherme Oliveira, Nithya Raghavan, Andrew Shedlock, Laurence Rodrigues do Amaral, Halime D Arican-Goktas, Juliana G Assis, Elio Hideo Baba, Olga L Baron, Christopher J Bayne, Utibe Bickham-Wright, Kyle K Biggar, Michael Blouin, Bryony C Bonning, Chris BotkaJoanna M Bridger, Katherine M Buckley, Sarah K Buddenborg, Roberta Lima Caldeira, Julia Carleton, Omar S Carvalho, Maria G Castillo, Iain W Chalmers, Mikkel Christensens, Sandra Clifton, Celine Cosseau, Christine Coustau, Richard M Cripps, Yesid Cuesta-Astroz, Scott F Cummins, Leon di Stephano, Nathalie Dinguirard, David Duval, Scott Emrich, Cédric Feschotte, Rene Feyereisen, Peter FitzGerald, Catrina Fronick, Lucinda Fulton, Richard Galinier, Sandra G Gava, Michael Geusz, Kathrin K Geyer, Gloria I Giraldo-Calderón, Matheus de Souza Gomes, Michelle A Gordy, Benjamin Gourbal, Christoph Grunau, Patrick C Hanington, Karl F Hoffmann, Daniel Hughes, Judith Humphries, Daniel J Jackson, Liana K Jannotti-Passos, Wander de Jesus Jeremias, Susan Jobling, Bishoy Kamel, Aurélie Kapusta, Satwant Kaur, Joris M Koene, Andrea B Kohn, Dan Lawson, Scott P Lawton, Di Liang, Yanin Limpanont, Sijun Liu, Anne E Lockyer, TyAnna L Lovato, Fernanda Ludolf, Vince Magrini, Donald P McManus, Monica Medina, Milind Misra, Guillaume Mitta, Gerald M Mkoji, Michael J Montague, Cesar Montelongo, Leonid L Moroz, Monica C Munoz-Torres, Umar Niazi, Leslie R Noble, Francislon S Oliveira, Fabiano S Pais, Anthony T Papenfuss, Rob Peace, Janeth J Pena, Emmanuel A Pila, Titouan Quelais, Brian J Raney, Jonathan P Rast, David Rollinson, Izinara C Rosse, Bronwyn Rotgans, Edwin J Routledge, Kathryn M Ryan, Larissa L S Scholte, Kenneth B Storey, Martin Swain, Jacob A Tennessen, Chad Tomlinson, Damian L Trujillo, Emanuela V Volpi, Anthony J Walker, Tianfang Wang, Ittiprasert Wannaporn, Wesley C Warren, Xiao-Jun Wu, Timothy P Yoshino, Mohammed Yusuf, Si-Ming Zhang, Min Zhao, Richard K Wilson

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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.

Original languageEnglish
Article number15451
Number of pages12
JournalNature Communications
Volume8
Early online date16 May 2017
DOIs
Publication statusPublished - 16 May 2017

Bibliographical note

Acknowledgements
We thank S. Newfeld for discussion of actin evolution; N. El Sayed and H. Tettelin for discussion of HSP annotation and expression. We acknowledge access to the Metafer microscopy system at the I. Robinson Research Complex, Harwell, Rutherford Appleton Laboratory, Oxon, UK (BBSRC Professorial Fellowship, grant number BB/H022597/1). Sequence characterization of the Biomphalaria glabrata genome was funded by NIH-NHGRI grant HG003079 to R.K.W., McDonnell Genome Institute, Washington University School of Medicine. Biomphalaria glabrata and Schistosoma mansoni were provided to some participating labs by the NIAID Schistosomiasis Resource Center (Biomedical Research Institute, Rockville, MD) through NIH-NIAID Contract HHSN272201000005I for distribution through BEI Resources. C.M.A. and E.S.L. acknowledge NIH grant P30GM110907 from the National Institute of General Medical Sciences (NIGMS). Publication costs were contributed equally by McDonnell Genome Institute, Washington University School of Medicine and the COBRE Center for Evolutionary and Theoretical Immunology (CETI) which is supported by NIH grant P30GM110907 from the National Institute of General Medical Sciences (NIGMS). E.S.L. acknowledges NIH/NIAID ROI AI101438. J.M.B., H.D.A.-G and M.K. acknowledge NIH-NIAID R01-AI0634808. M.Y. acknowledges UK BBSRC (BB/H022597/1). G.O. acknowledges support from FAPEMIG (RED-00014-14, PPM-00189-13) and CNPq (304138/2014-2, 309312/2012-4). R.L.C. acknowledges CNPq (503275/2011-5). T.P.Y. acknowledges NIH/NIAID RO1AI015503. K.F.H. and M.T.S. acknowledge BBSRC (BB/K005448/1). B.G. acknowledges ANR JCJC INVIMORY (ANR-13-JSV7-0009). S.E. acknowledges NIAID contract HHSN272201400029C. J.M.K. acknowledges the Research Council for Earth and Life Sciences (A.L.W.; 819.01.007) and the Netherlands Organization for Scientific Research (NWO). R.M.C. acknowledges NIH GM061738 and support from the American Heart Association, Southwest Affiliate (14GRNT20490250). D.T. acknowledges NIH R25 GM075149. C.F. acknowledges NIH R01-GM077582. D.J.J. acknowledges D.F.G. JA2108/1-2. M.de S.G. acknowledges CNPq 479890/2013-7. K.M.B. and J.P.R. acknowledge NSERC 312221 and CIHR MOP74667. C.S.J., L.R.N., S.J., E.J.R., S.K. and A.E.L. acknowledge NC3R GO900802/1. K.K.B. and K.B.S. acknowledge NSERC 315051 and 6793, respectively. M.B. and C.J.B. acknowledge NIH RO1-AI109134. C.J.B. acknowledges NIH AI016137 and AI111201. B.R. acknowledges NHGRI 4U41HG002371. P.C.H., M.A.G. and E.A.P. acknowledge NSERC 418540. O.L.B. and Ch.C. acknowledge ANR-12-EMMA-0007-01. S.F.C. acknowledges Australian Research Council FT110100990.

Keywords

  • Journal Article
  • DNA sequencing
  • genome
  • genome informatics
  • zoology

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