Unique features of a global human ectoparasite identified through sequencing of the bed bug genome

Joshua B. Benoit; Zach N. Adelman; Klaus Reinhardt; Amanda Dolan; Monica Poelchau; Emily C. Jennings; Elise M. Szuter; Richard W. Hagan; Hemant Gujar; Jayendra Nath Shukla; Fang Zhu; M. Mohan; David R. Nelson; Andrew J. Rosendale; Christian Derst; Valentina Resnik; Sebastian Wernig; Pamela Menegazzi; Christian Wegener; Nicolai Peschel; Jacob M. Hendershot; Wolfgang Blenau; Reinhard Predel; Paul R. Johnston; Panagiotis Ioannidis; Robert M. Waterhouse; Ralf Nauen; Corinna Schorn; Mark Christoph Ott; Frank Maiwald; J. Spencer Johnston; Ameya D. Gondhalekar; Michael E. Scharf; Brittany F. Peterson; Kapil R. Raje; Benjamin A. Hottel; David Armisén; Antonin Jean Johan Crumière; Peter Nagui Refki; Maria Emilia Santos; Essia Sghaier; Sèverine Viala; Abderrahman Khila; Seung Joon Ahn; Christopher Childers; Chien Yueh Lee; Han Lin; Daniel S.T. Hughes; Elizabeth J. Duncan; Shwetha C. Murali; Jiaxin Qu; Shannon Dugan; Sandra L. Lee; Hsu Chao; Huyen Dinh; Yi Han; Harshavardhan Doddapaneni; Kim C. Worley; Donna M. Muzny; David Wheeler; Kristen A. Panfilio; Iris M. Vargas Jentzsch; Edward L. Vargo; Warren Booth; Markus Friedrich; Matthew T. Weirauch; Michelle A.E. Anderson; Jeffery W. Jones; Omprakash Mittapalli; Chaoyang Zhao; Jing Jiang Zhou; Jay D. Evans; Geoffrey M. Attardo; Hugh M. Robertson; Evgeny M. Zdobnov; Jose M.C. Ribeiro; Richard A. Gibbs; John H. Werren; Subba R. Palli; Coby Schal; Stephen Richards

doi:10.1038/ncomms10165

Unique features of a global human ectoparasite identified through sequencing of the bed bug genome

Joshua B. Benoit, Zach N. Adelman, Klaus Reinhardt, Amanda Dolan, Monica Poelchau, Emily C. Jennings, Elise M. Szuter, Richard W. Hagan, Hemant Gujar, Jayendra Nath Shukla, Fang Zhu, M. Mohan, David R. Nelson, Andrew J. Rosendale, Christian Derst, Valentina Resnik, Sebastian Wernig, Pamela Menegazzi, Christian Wegener, Nicolai PeschelJacob M. Hendershot, Wolfgang Blenau, Reinhard Predel, Paul R. Johnston, Panagiotis Ioannidis, Robert M. Waterhouse, Ralf Nauen, Corinna Schorn, Mark Christoph Ott, Frank Maiwald, J. Spencer Johnston, Ameya D. Gondhalekar, Michael E. Scharf, Brittany F. Peterson, Kapil R. Raje, Benjamin A. Hottel, David Armisén, Antonin Jean Johan Crumière, Peter Nagui Refki, Maria Emilia Santos, Essia Sghaier, Sèverine Viala, Abderrahman Khila, Seung Joon Ahn, Christopher Childers, Chien Yueh Lee, Han Lin, Daniel S.T. Hughes, Elizabeth J. Duncan, Shwetha C. Murali, Jiaxin Qu, Shannon Dugan, Sandra L. Lee, Hsu Chao, Huyen Dinh, Yi Han, Harshavardhan Doddapaneni, Kim C. Worley, Donna M. Muzny, David Wheeler, Kristen A. Panfilio, Iris M. Vargas Jentzsch, Edward L. Vargo, Warren Booth, Markus Friedrich, Matthew T. Weirauch, Michelle A.E. Anderson, Jeffery W. Jones, Omprakash Mittapalli, Chaoyang Zhao, Jing Jiang Zhou, Jay D. Evans, Geoffrey M. Attardo, Hugh M. Robertson, Evgeny M. Zdobnov, Jose M.C. Ribeiro, Richard A. Gibbs, John H. Werren, Subba R. Palli, Coby Schal, Stephen Richards

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

126 Scopus citations

Abstract

The bed bug, Cimex lectularius, has re-established itself as a ubiquitous human ectoparasite throughout much of the world during the past two decades. This global resurgence is likely linked to increased international travel and commerce in addition to widespread insecticide resistance. Analyses of the C. lectularius sequenced genome (650 Mb) and 14,220 predicted protein-coding genes provide a comprehensive representation of genes that are linked to traumatic insemination, a reduced chemosensory repertoire of genes related to obligate hematophagy, host-symbiont interactions, and several mechanisms of insecticide resistance. In addition, we document the presence of multiple putative lateral gene transfer events. Genome sequencing and annotation establish a solid foundation for future research on mechanisms of insecticide resistance, human-bed bug and symbiont-bed bug associations, and unique features of bed bug biology that contribute to the unprecedented success of C. lectularius as a human ectoparasite.

Original language	English
Article number	10165
Journal	Nature Communications
Volume	7
DOIs	https://doi.org/10.1038/ncomms10165
State	Published - Feb 2 2016

Bibliographical note

Funding Information:
Funding for genome sequencing, assembly and automated annotation was provided by NHGRI grant U54 HG003273 to R.A.G. Funding for bed bug lines development was provided by Blanton J. Whitmire endowment, Housing and Urban Development (NCHHU-00017-13), National Science Foundation (IOS-1052238), Alfred P. Sloan Foundation (2013-5-35 MBE) to Cob. S. Funding for preparation of genomic DNA and RNA for sequencing and for manual curation of some of the genes was provided by NIH (GM070559-9) to S.R.P. Funding for manual curation and other analyses were provided by the Royal Society of New Zealand Marsden Fast Start Grant (11-UOO-124) to E.J.D., Fralin Life Sciences Institutes and Virginia Agriculture Experimental Station to Z.N.A., European Research Council (ERC-CoG 616346) to A.K., Deutsche For-schungsgemeinschaft (DFG): Pe1798/2-1 to N.P., Deutsche Forschungsgemeinschaft (DFG): PA2044/1-1 to K.A.P., Deutsche Forschungsgemeinschaft (DFG): collaborative research center SFB 1047 ‘Insect timing,’ Project A1 to P.M., The Zukunftskonzept at TU Dresden funded by the Exzellenzinitiative of the Deutsche Forschungsgemeinschaft to K.R., Deutsche Forschungsgemeinschaft (DFG): BL469/7-1 to Wo.B., Deutsche For-schungsgemeinschaft (DFG): 766/11-1 to R.P., European Research Council grant 260986 to P.J., Biotechnology and Biological Sciences Research Council to J.-J.Z., University of Cincinnati Faculty Development Research Grant and Ohio Supercomputer Center Research Allocation to J.B.B., Marie Curie International Outgoing Fellowship PIOF-GA-2011–303312 to R.M.W., National Science Foundation (DEB-1257053) to J.H.W., and Swiss National Science Foundation awards 31003A-125350 and 31003A-143936 to E.M.Z. We thank Rick Santangelo for generating the full-sib mating line used in this project. Given the restriction in the number of citations, it was not possible include all publications associated with programs used in this study. As an alternative, we have provided links to websites for each program. i5k genome sequencing initiative assisting in the sequencing of the bed bug genome.

Publisher Copyright:
© 2016, Nature Publishing Group. All rights reserved.

ASJC Scopus subject areas

Physics and Astronomy (all)
Chemistry (all)
Biochemistry, Genetics and Molecular Biology (all)

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10.1038/ncomms10165

Cite this

Benoit, J. B., Adelman, Z. N., Reinhardt, K., Dolan, A., Poelchau, M., Jennings, E. C., Szuter, E. M., Hagan, R. W., Gujar, H., Shukla, J. N., Zhu, F., Mohan, M., Nelson, D. R., Rosendale, A. J., Derst, C., Resnik, V., Wernig, S., Menegazzi, P., Wegener, C., ... Richards, S. (2016). Unique features of a global human ectoparasite identified through sequencing of the bed bug genome. Nature Communications, 7, [10165]. https://doi.org/10.1038/ncomms10165

@article{6e60b0c4863840819b47a8c3c885e6e6,

title = "Unique features of a global human ectoparasite identified through sequencing of the bed bug genome",

abstract = "The bed bug, Cimex lectularius, has re-established itself as a ubiquitous human ectoparasite throughout much of the world during the past two decades. This global resurgence is likely linked to increased international travel and commerce in addition to widespread insecticide resistance. Analyses of the C. lectularius sequenced genome (650 Mb) and 14,220 predicted protein-coding genes provide a comprehensive representation of genes that are linked to traumatic insemination, a reduced chemosensory repertoire of genes related to obligate hematophagy, host-symbiont interactions, and several mechanisms of insecticide resistance. In addition, we document the presence of multiple putative lateral gene transfer events. Genome sequencing and annotation establish a solid foundation for future research on mechanisms of insecticide resistance, human-bed bug and symbiont-bed bug associations, and unique features of bed bug biology that contribute to the unprecedented success of C. lectularius as a human ectoparasite.",

author = "Benoit, {Joshua B.} and Adelman, {Zach N.} and Klaus Reinhardt and Amanda Dolan and Monica Poelchau and Jennings, {Emily C.} and Szuter, {Elise M.} and Hagan, {Richard W.} and Hemant Gujar and Shukla, {Jayendra Nath} and Fang Zhu and M. Mohan and Nelson, {David R.} and Rosendale, {Andrew J.} and Christian Derst and Valentina Resnik and Sebastian Wernig and Pamela Menegazzi and Christian Wegener and Nicolai Peschel and Hendershot, {Jacob M.} and Wolfgang Blenau and Reinhard Predel and Johnston, {Paul R.} and Panagiotis Ioannidis and Waterhouse, {Robert M.} and Ralf Nauen and Corinna Schorn and Ott, {Mark Christoph} and Frank Maiwald and Johnston, {J. Spencer} and Gondhalekar, {Ameya D.} and Scharf, {Michael E.} and Peterson, {Brittany F.} and Raje, {Kapil R.} and Hottel, {Benjamin A.} and David Armis{\'e}n and Crumi{\`e}re, {Antonin Jean Johan} and Refki, {Peter Nagui} and Santos, {Maria Emilia} and Essia Sghaier and S{\`e}verine Viala and Abderrahman Khila and Ahn, {Seung Joon} and Christopher Childers and Lee, {Chien Yueh} and Han Lin and Hughes, {Daniel S.T.} and Duncan, {Elizabeth J.} and Murali, {Shwetha C.} and Jiaxin Qu and Shannon Dugan and Lee, {Sandra L.} and Hsu Chao and Huyen Dinh and Yi Han and Harshavardhan Doddapaneni and Worley, {Kim C.} and Muzny, {Donna M.} and David Wheeler and Panfilio, {Kristen A.} and {Vargas Jentzsch}, {Iris M.} and Vargo, {Edward L.} and Warren Booth and Markus Friedrich and Weirauch, {Matthew T.} and Anderson, {Michelle A.E.} and Jones, {Jeffery W.} and Omprakash Mittapalli and Chaoyang Zhao and Zhou, {Jing Jiang} and Evans, {Jay D.} and Attardo, {Geoffrey M.} and Robertson, {Hugh M.} and Zdobnov, {Evgeny M.} and Ribeiro, {Jose M.C.} and Gibbs, {Richard A.} and Werren, {John H.} and Palli, {Subba R.} and Coby Schal and Stephen Richards",

note = "Funding Information: Funding for genome sequencing, assembly and automated annotation was provided by NHGRI grant U54 HG003273 to R.A.G. Funding for bed bug lines development was provided by Blanton J. Whitmire endowment, Housing and Urban Development (NCHHU-00017-13), National Science Foundation (IOS-1052238), Alfred P. Sloan Foundation (2013-5-35 MBE) to Cob. S. Funding for preparation of genomic DNA and RNA for sequencing and for manual curation of some of the genes was provided by NIH (GM070559-9) to S.R.P. Funding for manual curation and other analyses were provided by the Royal Society of New Zealand Marsden Fast Start Grant (11-UOO-124) to E.J.D., Fralin Life Sciences Institutes and Virginia Agriculture Experimental Station to Z.N.A., European Research Council (ERC-CoG 616346) to A.K., Deutsche For-schungsgemeinschaft (DFG): Pe1798/2-1 to N.P., Deutsche Forschungsgemeinschaft (DFG): PA2044/1-1 to K.A.P., Deutsche Forschungsgemeinschaft (DFG): collaborative research center SFB 1047 {\textquoteleft}Insect timing,{\textquoteright} Project A1 to P.M., The Zukunftskonzept at TU Dresden funded by the Exzellenzinitiative of the Deutsche Forschungsgemeinschaft to K.R., Deutsche Forschungsgemeinschaft (DFG): BL469/7-1 to Wo.B., Deutsche For-schungsgemeinschaft (DFG): 766/11-1 to R.P., European Research Council grant 260986 to P.J., Biotechnology and Biological Sciences Research Council to J.-J.Z., University of Cincinnati Faculty Development Research Grant and Ohio Supercomputer Center Research Allocation to J.B.B., Marie Curie International Outgoing Fellowship PIOF-GA-2011–303312 to R.M.W., National Science Foundation (DEB-1257053) to J.H.W., and Swiss National Science Foundation awards 31003A-125350 and 31003A-143936 to E.M.Z. We thank Rick Santangelo for generating the full-sib mating line used in this project. Given the restriction in the number of citations, it was not possible include all publications associated with programs used in this study. As an alternative, we have provided links to websites for each program. i5k genome sequencing initiative assisting in the sequencing of the bed bug genome. Publisher Copyright: {\textcopyright} 2016, Nature Publishing Group. All rights reserved.",

year = "2016",

month = feb,

day = "2",

doi = "10.1038/ncomms10165",

language = "English",

volume = "7",

}

Benoit, JB, Adelman, ZN, Reinhardt, K, Dolan, A, Poelchau, M, Jennings, EC, Szuter, EM, Hagan, RW, Gujar, H, Shukla, JN, Zhu, F, Mohan, M, Nelson, DR, Rosendale, AJ, Derst, C, Resnik, V, Wernig, S, Menegazzi, P, Wegener, C, Peschel, N, Hendershot, JM, Blenau, W, Predel, R, Johnston, PR, Ioannidis, P, Waterhouse, RM, Nauen, R, Schorn, C, Ott, MC, Maiwald, F, Johnston, JS, Gondhalekar, AD, Scharf, ME, Peterson, BF, Raje, KR, Hottel, BA, Armisén, D, Crumière, AJJ, Refki, PN, Santos, ME, Sghaier, E, Viala, S, Khila, A, Ahn, SJ, Childers, C, Lee, CY, Lin, H, Hughes, DST, Duncan, EJ, Murali, SC, Qu, J, Dugan, S, Lee, SL, Chao, H, Dinh, H, Han, Y, Doddapaneni, H, Worley, KC, Muzny, DM, Wheeler, D, Panfilio, KA, Vargas Jentzsch, IM, Vargo, EL, Booth, W, Friedrich, M, Weirauch, MT, Anderson, MAE, Jones, JW, Mittapalli, O, Zhao, C, Zhou, JJ, Evans, JD, Attardo, GM, Robertson, HM, Zdobnov, EM, Ribeiro, JMC, Gibbs, RA, Werren, JH, Palli, SR, Schal, C & Richards, S 2016, 'Unique features of a global human ectoparasite identified through sequencing of the bed bug genome', Nature Communications, vol. 7, 10165. https://doi.org/10.1038/ncomms10165

TY - JOUR

T1 - Unique features of a global human ectoparasite identified through sequencing of the bed bug genome

AU - Benoit, Joshua B.

AU - Adelman, Zach N.

AU - Reinhardt, Klaus

AU - Dolan, Amanda

AU - Poelchau, Monica

AU - Jennings, Emily C.

AU - Szuter, Elise M.

AU - Hagan, Richard W.

AU - Gujar, Hemant

AU - Shukla, Jayendra Nath

AU - Zhu, Fang

AU - Mohan, M.

AU - Nelson, David R.

AU - Rosendale, Andrew J.

AU - Derst, Christian

AU - Resnik, Valentina

AU - Wernig, Sebastian

AU - Menegazzi, Pamela

AU - Wegener, Christian

AU - Peschel, Nicolai

AU - Hendershot, Jacob M.

AU - Blenau, Wolfgang

AU - Predel, Reinhard

AU - Johnston, Paul R.

AU - Ioannidis, Panagiotis

AU - Waterhouse, Robert M.

AU - Nauen, Ralf

AU - Schorn, Corinna

AU - Ott, Mark Christoph

AU - Maiwald, Frank

AU - Johnston, J. Spencer

AU - Gondhalekar, Ameya D.

AU - Scharf, Michael E.

AU - Peterson, Brittany F.

AU - Raje, Kapil R.

AU - Hottel, Benjamin A.

AU - Armisén, David

AU - Crumière, Antonin Jean Johan

AU - Refki, Peter Nagui

AU - Santos, Maria Emilia

AU - Sghaier, Essia

AU - Viala, Sèverine

AU - Khila, Abderrahman

AU - Ahn, Seung Joon

AU - Childers, Christopher

AU - Lee, Chien Yueh

AU - Lin, Han

AU - Hughes, Daniel S.T.

AU - Duncan, Elizabeth J.

AU - Murali, Shwetha C.

AU - Qu, Jiaxin

AU - Dugan, Shannon

AU - Lee, Sandra L.

AU - Chao, Hsu

AU - Dinh, Huyen

AU - Han, Yi

AU - Doddapaneni, Harshavardhan

AU - Worley, Kim C.

AU - Muzny, Donna M.

AU - Wheeler, David

AU - Panfilio, Kristen A.

AU - Vargas Jentzsch, Iris M.

AU - Vargo, Edward L.

AU - Booth, Warren

AU - Friedrich, Markus

AU - Weirauch, Matthew T.

AU - Anderson, Michelle A.E.

AU - Jones, Jeffery W.

AU - Mittapalli, Omprakash

AU - Zhao, Chaoyang

AU - Zhou, Jing Jiang

AU - Evans, Jay D.

AU - Attardo, Geoffrey M.

AU - Robertson, Hugh M.

AU - Zdobnov, Evgeny M.

AU - Ribeiro, Jose M.C.

AU - Gibbs, Richard A.

AU - Werren, John H.

AU - Palli, Subba R.

AU - Schal, Coby

AU - Richards, Stephen

N1 - Funding Information: Funding for genome sequencing, assembly and automated annotation was provided by NHGRI grant U54 HG003273 to R.A.G. Funding for bed bug lines development was provided by Blanton J. Whitmire endowment, Housing and Urban Development (NCHHU-00017-13), National Science Foundation (IOS-1052238), Alfred P. Sloan Foundation (2013-5-35 MBE) to Cob. S. Funding for preparation of genomic DNA and RNA for sequencing and for manual curation of some of the genes was provided by NIH (GM070559-9) to S.R.P. Funding for manual curation and other analyses were provided by the Royal Society of New Zealand Marsden Fast Start Grant (11-UOO-124) to E.J.D., Fralin Life Sciences Institutes and Virginia Agriculture Experimental Station to Z.N.A., European Research Council (ERC-CoG 616346) to A.K., Deutsche For-schungsgemeinschaft (DFG): Pe1798/2-1 to N.P., Deutsche Forschungsgemeinschaft (DFG): PA2044/1-1 to K.A.P., Deutsche Forschungsgemeinschaft (DFG): collaborative research center SFB 1047 ‘Insect timing,’ Project A1 to P.M., The Zukunftskonzept at TU Dresden funded by the Exzellenzinitiative of the Deutsche Forschungsgemeinschaft to K.R., Deutsche Forschungsgemeinschaft (DFG): BL469/7-1 to Wo.B., Deutsche For-schungsgemeinschaft (DFG): 766/11-1 to R.P., European Research Council grant 260986 to P.J., Biotechnology and Biological Sciences Research Council to J.-J.Z., University of Cincinnati Faculty Development Research Grant and Ohio Supercomputer Center Research Allocation to J.B.B., Marie Curie International Outgoing Fellowship PIOF-GA-2011–303312 to R.M.W., National Science Foundation (DEB-1257053) to J.H.W., and Swiss National Science Foundation awards 31003A-125350 and 31003A-143936 to E.M.Z. We thank Rick Santangelo for generating the full-sib mating line used in this project. Given the restriction in the number of citations, it was not possible include all publications associated with programs used in this study. As an alternative, we have provided links to websites for each program. i5k genome sequencing initiative assisting in the sequencing of the bed bug genome. Publisher Copyright: © 2016, Nature Publishing Group. All rights reserved.

PY - 2016/2/2

Y1 - 2016/2/2

N2 - The bed bug, Cimex lectularius, has re-established itself as a ubiquitous human ectoparasite throughout much of the world during the past two decades. This global resurgence is likely linked to increased international travel and commerce in addition to widespread insecticide resistance. Analyses of the C. lectularius sequenced genome (650 Mb) and 14,220 predicted protein-coding genes provide a comprehensive representation of genes that are linked to traumatic insemination, a reduced chemosensory repertoire of genes related to obligate hematophagy, host-symbiont interactions, and several mechanisms of insecticide resistance. In addition, we document the presence of multiple putative lateral gene transfer events. Genome sequencing and annotation establish a solid foundation for future research on mechanisms of insecticide resistance, human-bed bug and symbiont-bed bug associations, and unique features of bed bug biology that contribute to the unprecedented success of C. lectularius as a human ectoparasite.

AB - The bed bug, Cimex lectularius, has re-established itself as a ubiquitous human ectoparasite throughout much of the world during the past two decades. This global resurgence is likely linked to increased international travel and commerce in addition to widespread insecticide resistance. Analyses of the C. lectularius sequenced genome (650 Mb) and 14,220 predicted protein-coding genes provide a comprehensive representation of genes that are linked to traumatic insemination, a reduced chemosensory repertoire of genes related to obligate hematophagy, host-symbiont interactions, and several mechanisms of insecticide resistance. In addition, we document the presence of multiple putative lateral gene transfer events. Genome sequencing and annotation establish a solid foundation for future research on mechanisms of insecticide resistance, human-bed bug and symbiont-bed bug associations, and unique features of bed bug biology that contribute to the unprecedented success of C. lectularius as a human ectoparasite.

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UR - http://www.scopus.com/inward/citedby.url?scp=84957602748&partnerID=8YFLogxK

U2 - 10.1038/ncomms10165

DO - 10.1038/ncomms10165

M3 - Article

C2 - 26836814

AN - SCOPUS:84957602748

VL - 7

M1 - 10165

ER -

Unique features of a global human ectoparasite identified through sequencing of the bed bug genome

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