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 Botka & 97 others 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, 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
JournalNature Communications
Volume8
DOIs
Publication statusPublished - 16 May 2017

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snails
genome
Schistosomiasis
Snails
Fresh Water
Genes
Genome
Biomphalaria
Medical problems
Gene expression
Schistosoma mansoni
Blood
Health
health
Trematoda
gene expression
Gene Expression Regulation
biology
blood

Keywords

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

Cite this

Adema, C. M., Hillier, L. W., Jones, C. S., Loker, E. S., Knight, M., Minx, P., ... Wilson, R. K. (2017). Whole genome analysis of a schistosomiasis-transmitting freshwater snail. Nature Communications, 8, [15451]. https://doi.org/10.1038/ncomms15451

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

In: Nature Communications, Vol. 8, 15451, 16.05.2017.

Research output: Contribution to journalArticle

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 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, TL, 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, X-J, Yoshino, TP, Yusuf, M, Zhang, S-M, Zhao, M & Wilson, RK 2017, 'Whole genome analysis of a schistosomiasis-transmitting freshwater snail', Nature Communications, vol. 8, 15451. https://doi.org/10.1038/ncomms15451
Adema, Coen M ; Hillier, LaDeana W ; Jones, Catherine S ; Loker, Eric S ; Knight, Matty ; Minx, Patrick ; Oliveira, Guilherme ; Raghavan, Nithya ; Shedlock, Andrew ; do Amaral, Laurence Rodrigues ; Arican-Goktas, Halime D ; Assis, Juliana G ; Baba, Elio Hideo ; Baron, Olga L ; Bayne, Christopher J ; Bickham-Wright, Utibe ; Biggar, Kyle K ; Blouin, Michael ; Bonning, Bryony C ; Botka, Chris ; Bridger, Joanna M ; Buckley, Katherine M ; Buddenborg, Sarah K ; Lima Caldeira, Roberta ; Carleton, Julia ; Carvalho, Omar S ; Castillo, Maria G ; Chalmers, Iain W ; Christensens, Mikkel ; Clifton, Sandra ; Cosseau, Celine ; Coustau, Christine ; Cripps, Richard M ; Cuesta-Astroz, Yesid ; Cummins, Scott F ; di Stephano, Leon ; Dinguirard, Nathalie ; Duval, David ; Emrich, Scott ; Feschotte, Cédric ; Feyereisen, Rene ; FitzGerald, Peter ; Fronick, Catrina ; Fulton, Lucinda ; Galinier, Richard ; Gava, Sandra G ; Geusz, Michael ; Geyer, Kathrin K ; Giraldo-Calderón, Gloria I ; de Souza Gomes, Matheus ; Gordy, Michelle A ; Gourbal, Benjamin ; Grunau, Christoph ; Hanington, Patrick C ; Hoffmann, Karl F ; Hughes, Daniel ; Humphries, Judith ; Jackson, Daniel J ; Jannotti-Passos, Liana K ; de Jesus Jeremias, Wander ; Jobling, Susan ; Kamel, Bishoy ; Kapusta, Aurélie ; Kaur, Satwant ; Koene, Joris M ; Kohn, Andrea B ; Lawson, Dan ; Lawton, Scott P ; Liang, Di ; Limpanont, Yanin ; Liu, Sijun ; Lockyer, Anne E ; Lovato, TyAnna L ; Ludolf, Fernanda ; Magrini, Vince ; McManus, Donald P ; Medina, Monica ; Misra, Milind ; Mitta, Guillaume ; Mkoji, Gerald M ; Montague, Michael J ; Montelongo, Cesar ; Moroz, Leonid L ; Munoz-Torres, Monica C ; Niazi, Umar ; Noble, Leslie R ; Oliveira, Francislon S ; Pais, Fabiano S ; Papenfuss, Anthony T ; Peace, Rob ; Pena, Janeth J ; Pila, Emmanuel A ; Quelais, Titouan ; Raney, Brian J ; Rast, Jonathan P ; Rollinson, David ; Rosse, Izinara C ; Rotgans, Bronwyn ; Routledge, Edwin J ; Ryan, Kathryn M ; Scholte, Larissa L S ; Storey, Kenneth B ; Swain, Martin ; Tennessen, Jacob A ; Tomlinson, Chad ; Trujillo, Damian L ; Volpi, Emanuela V ; Walker, Anthony J ; Wang, Tianfang ; Wannaporn, Ittiprasert ; Warren, Wesley C ; Wu, Xiao-Jun ; Yoshino, Timothy P ; Yusuf, Mohammed ; Zhang, Si-Ming ; Zhao, Min ; Wilson, Richard K. / Whole genome analysis of a schistosomiasis-transmitting freshwater snail. In: Nature Communications. 2017 ; Vol. 8.
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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 = "Journal Article, DNA sequencing, genome, genome informatics, zoology",
author = "Adema, {Coen M} and Hillier, {LaDeana 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, {TyAnna 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 Xiao-Jun Wu and Yoshino, {Timothy P} and Mohammed Yusuf and Si-Ming Zhang and Min Zhao and Wilson, {Richard K}",
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.",
year = "2017",
month = "5",
day = "16",
doi = "10.1038/ncomms15451",
language = "English",
volume = "8",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "Nature Publishing Group",

}

TY - JOUR

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

AU - Adema, Coen M

AU - Hillier, LaDeana 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, TyAnna 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 - 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.

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 - Journal Article

KW - DNA sequencing

KW - genome

KW - genome informatics

KW - zoology

U2 - 10.1038/ncomms15451

DO - 10.1038/ncomms15451

M3 - Article

VL - 8

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

M1 - 15451

ER -