Whole genome analysis of a schistosomiasis-transmitting freshwater snail

Coen M. Adema; La Deana 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 Botka; Joanna 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; Ty Anna 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

doi:10.1038/ncomms15451

Whole genome analysis of a schistosomiasis-transmitting freshwater snail

Coen M. Adema
, La Deana 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 Botka

Joanna 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, Ty Anna 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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Fundação Oswaldo Cruz
Instituto Tecnológico Vale
Medical University of South Carolina
Universidade Federal de Uberlândia
Brunel University London
CNRS
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Carleton University
Iowa State University
Harvard University
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University of Utah
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Aberystwyth University
European Molecular Biology Laboratory
Université de Perpignan
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Walter and Eliza Hall Institute of Medical Research
Peter Maccallum Cancer Centre
University of Notre Dame
University of Copenhagen
National Institutes of Health
Bowling Green State University
University of Alberta
Lawrence University
University of Göttingen
Pennsylvania State University
Vrije Universiteit Amsterdam
University of Florida
Kingston University
Queensland Institute of Medical Research
Kenya Medical Research Institute
University of Pennsylvania
Lawrence Berkeley National Laboratory
University of California at Santa Cruz
The Natural History Museum, London
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Rutherford Appelton Laboratory

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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 language	English
Journal	Nature Communications
Volume	8
Issue number	15451
DOIs	https://doi.org/10.1038/ncomms15451
Publication status	Published - 16 May 2017

Bibliographical note

Note: 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.

Keywords

Biological sciences

Access to Document

10.1038/ncomms15451

Lawton S 38227 VoRFinal published version, 1.47 MBLicence: CC BY

http://dx.doi.org/10.1038/ncomms15451

Cite this

Adema, C. M., Hillier, L. D. W., Jones, C. S., Loker, E. S., Knight, M., Minx, P., Oliveira, G., Raghavan, N., Shedlock, A., Do Amaral, L. R., Arican-Goktas, H. D., Assis, J. G., Baba, E. H., Baron, O. L., Bayne, C. J., Bickham-Wright, U., Biggar, K. K., Blouin, M., Bonning, B. C., ... Wilson, R. K. (2017). Whole genome analysis of a schistosomiasis-transmitting freshwater snail. Nature Communications, 8(15451). https://doi.org/10.1038/ncomms15451

@article{d6dee179a27d478d8e21667d8b2aa5d4,

title = "Whole genome analysis of a schistosomiasis-transmitting freshwater snail",

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.",

keywords = "Biological sciences",

author = "Adema, \{Coen M.\} and Hillier, \{La Deana W.\} and Jones, \{Catherine S.\} and Loker, \{Eric S.\} and Matty Knight and Patrick Minx and Guilherme Oliveira and Nithya Raghavan and Andrew Shedlock and \{Do Amaral\}, \{Laurence Rodrigues\} and Arican-Goktas, \{Halime D.\} and Assis, \{Juliana G.\} and Baba, \{Elio Hideo\} and Baron, \{Olga L.\} and Bayne, \{Christopher J.\} and Utibe Bickham-Wright and Biggar, \{Kyle K.\} and Michael Blouin and Bonning, \{Bryony C.\} and Chris Botka and Bridger, \{Joanna M.\} and Buckley, \{Katherine M.\} and Buddenborg, \{Sarah K.\} and \{Lima Caldeira\}, Roberta and Julia Carleton and Carvalho, \{Omar S.\} and Castillo, \{Maria G.\} and Chalmers, \{Iain W.\} and Mikkel Christensens and Sandra Clifton and Celine Cosseau and Christine Coustau and Cripps, \{Richard M.\} and Yesid Cuesta-Astroz and Cummins, \{Scott F.\} and \{DI Stephano\}, Leon and Nathalie DInguirard and David Duval and Scott Emrich and C{\'e}dric Feschotte and Rene Feyereisen and Peter Fitzgerald and Catrina Fronick and Lucinda Fulton and Richard Galinier and Gava, \{Sandra G.\} and Michael Geusz and Geyer, \{Kathrin K.\} and Giraldo-Calder{\'o}n, \{Gloria I.\} and \{De Souza Gomes\}, Matheus and Gordy, \{Michelle A.\} and Benjamin Gourbal and Christoph Grunau and Hanington, \{Patrick C.\} and Hoffmann, \{Karl F.\} and Daniel Hughes and Judith Humphries and Jackson, \{Daniel J.\} and Jannotti-Passos, \{Liana K.\} and \{De Jesus Jeremias\}, Wander and Susan Jobling and Bishoy Kamel and Aur{\'e}lie Kapusta and Satwant Kaur and Koene, \{Joris M.\} and Kohn, \{Andrea B.\} and Dan Lawson and Lawton, \{Scott P.\} and Di Liang and Yanin Limpanont and Sijun Liu and Lockyer, \{Anne E.\} and Lovato, \{Ty Anna L.\} and Fernanda Ludolf and Vince Magrini and McManus, \{Donald P.\} and Monica Medina and Milind Misra and Guillaume Mitta and Mkoji, \{Gerald M.\} and Montague, \{Michael J.\} and Cesar Montelongo and Moroz, \{Leonid L.\} and Munoz-Torres, \{Monica C.\} and Umar Niazi and Noble, \{Leslie R.\} and Oliveira, \{Francislon S.\} and Pais, \{Fabiano S.\} and Papenfuss, \{Anthony T.\} and Rob Peace and Pena, \{Janeth J.\} and Pila, \{Emmanuel A.\} and Titouan Quelais and Raney, \{Brian J.\} and Rast, \{Jonathan P.\} and David Rollinson and Rosse, \{Izinara C.\} and Bronwyn Rotgans and Routledge, \{Edwin J.\} and Ryan, \{Kathryn M.\} and Scholte, \{Larissa L.S.\} and Storey, \{Kenneth B.\} and Martin Swain and Tennessen, \{Jacob A.\} and Chad Tomlinson and Trujillo, \{Damian L.\} and Volpi, \{Emanuela V.\} and Walker, \{Anthony J.\} and Tianfang Wang and Ittiprasert Wannaporn and Warren, \{Wesley C.\} and Wu, \{Xiao Jun\} and Yoshino, \{Timothy P.\} and Mohammed Yusuf and Zhang, \{Si Ming\} and Min Zhao and Wilson, \{Richard K.\}",

note = "Note: 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.",

year = "2017",

month = may,

day = "16",

doi = "10.1038/ncomms15451",

language = "English",

volume = "8",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Research",

number = "15451",

}

Adema, CM, Hillier, LDW, 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 Stephano, 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, Swain, M, Tennessen, JA, Tomlinson, C, Trujillo, DL, Volpi, EV, Walker, AJ, Wang, T, Wannaporn, I, Warren, WC, Wu, XJ, Yoshino, TP, Yusuf, M, Zhang, SM, Zhao, M & Wilson, RK 2017, 'Whole genome analysis of a schistosomiasis-transmitting freshwater snail', Nature Communications, vol. 8, no. 15451. https://doi.org/10.1038/ncomms15451

TY - JOUR

T1 - Whole genome analysis of a schistosomiasis-transmitting freshwater snail

AU - Adema, Coen M.

AU - Hillier, La Deana W.

AU - Jones, Catherine S.

AU - Loker, Eric S.

AU - Knight, Matty

AU - Minx, Patrick

AU - Oliveira, Guilherme

AU - Raghavan, Nithya

AU - Shedlock, Andrew

AU - Do Amaral, Laurence Rodrigues

AU - Arican-Goktas, Halime D.

AU - Assis, Juliana G.

AU - Baba, Elio Hideo

AU - Baron, Olga L.

AU - Bayne, Christopher J.

AU - Bickham-Wright, Utibe

AU - Biggar, Kyle K.

AU - Blouin, Michael

AU - Bonning, Bryony C.

AU - Botka, Chris

AU - Bridger, Joanna M.

AU - Buckley, Katherine M.

AU - Buddenborg, Sarah K.

AU - Lima Caldeira, Roberta

AU - Carleton, Julia

AU - Carvalho, Omar S.

AU - Castillo, Maria G.

AU - Chalmers, Iain W.

AU - Christensens, Mikkel

AU - Clifton, Sandra

AU - Cosseau, Celine

AU - Coustau, Christine

AU - Cripps, Richard M.

AU - Cuesta-Astroz, Yesid

AU - Cummins, Scott F.

AU - DI Stephano, Leon

AU - DInguirard, Nathalie

AU - Duval, David

AU - Emrich, Scott

AU - Feschotte, Cédric

AU - Feyereisen, Rene

AU - Fitzgerald, Peter

AU - Fronick, Catrina

AU - Fulton, Lucinda

AU - Galinier, Richard

AU - Gava, Sandra G.

AU - Geusz, Michael

AU - Geyer, Kathrin K.

AU - Giraldo-Calderón, Gloria I.

AU - De Souza Gomes, Matheus

AU - Gordy, Michelle A.

AU - Gourbal, Benjamin

AU - Grunau, Christoph

AU - Hanington, Patrick C.

AU - Hoffmann, Karl F.

AU - Hughes, Daniel

AU - Humphries, Judith

AU - Jackson, Daniel J.

AU - Jannotti-Passos, Liana K.

AU - De Jesus Jeremias, Wander

AU - Jobling, Susan

AU - Kamel, Bishoy

AU - Kapusta, Aurélie

AU - Kaur, Satwant

AU - Koene, Joris M.

AU - Kohn, Andrea B.

AU - Lawson, Dan

AU - Lawton, Scott P.

AU - Liang, Di

AU - Limpanont, Yanin

AU - Liu, Sijun

AU - Lockyer, Anne E.

AU - Lovato, Ty Anna L.

AU - Ludolf, Fernanda

AU - Magrini, Vince

AU - McManus, Donald P.

AU - Medina, Monica

AU - Misra, Milind

AU - Mitta, Guillaume

AU - Mkoji, Gerald M.

AU - Montague, Michael J.

AU - Montelongo, Cesar

AU - Moroz, Leonid L.

AU - Munoz-Torres, Monica C.

AU - Niazi, Umar

AU - Noble, Leslie R.

AU - Oliveira, Francislon S.

AU - Pais, Fabiano S.

AU - Papenfuss, Anthony T.

AU - Peace, Rob

AU - Pena, Janeth J.

AU - Pila, Emmanuel A.

AU - Quelais, Titouan

AU - Raney, Brian J.

AU - Rast, Jonathan P.

AU - Rollinson, David

AU - Rosse, Izinara C.

AU - Rotgans, Bronwyn

AU - Routledge, Edwin J.

AU - Ryan, Kathryn M.

AU - Scholte, Larissa L.S.

AU - Storey, Kenneth B.

AU - Swain, Martin

AU - Tennessen, Jacob A.

AU - Tomlinson, Chad

AU - Trujillo, Damian L.

AU - Volpi, Emanuela V.

AU - Walker, Anthony J.

AU - Wang, Tianfang

AU - Wannaporn, Ittiprasert

AU - Warren, Wesley C.

AU - Wu, Xiao Jun

AU - Yoshino, Timothy P.

AU - Yusuf, Mohammed

AU - Zhang, Si Ming

AU - Zhao, Min

AU - Wilson, Richard K.

N1 - Note: 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.

PY - 2017/5/16

Y1 - 2017/5/16

N2 - 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.

AB - 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.

KW - Biological sciences

UR - http://www.ncbi.nlm.nih.gov/pubmed/28508897

U2 - 10.1038/ncomms15451

DO - 10.1038/ncomms15451

M3 - Article

C2 - 28508897

SN - 2041-1723

VL - 8

JO - Nature Communications

JF - Nature Communications

IS - 15451

ER -

Whole genome analysis of a schistosomiasis-transmitting freshwater snail

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