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Research Article

Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle

Ewen F. Kirkness, Brian J. Haas, Weilin Sun, Henk R. Braig, M. Alejandra Perotti, John M. Clark, Si Hyeock Lee, Hugh M. Robertson, Ryan C. Kennedy, Eran Elhaik, Daniel Gerlach, Evgenia V. Kriventseva, Christine G. Elsik, Dan Graur, Catherine A. Hill, Jan A. Veenstra, Brian Walenz, José Manuel C. Tubío, José M. C. Ribeiro, Julio Rozas, J. Spencer Johnston, Justin T. Reese, Aleksandar Popadic, Marta Tojo, Didier Raoult, David L. Reed, Yoshinori Tomoyasu, Emily Krause, Omprakash Mittapalli, Venu M. Margam, Hong-Mei Li, Jason M. Meyer, Reed M. Johnson, Jeanne Romero-Severson, Janice Pagel VanZee, David Alvarez-Ponce, Filipe G. Vieira, Montserrat Aguadé, Sara Guirao-Rico, Juan M. Anzola, Kyong S. Yoon, Joseph P. Strycharz, Maria F. Unger, Scott Christley, Neil F. Lobo, Manfredo J. Seufferheld, NaiKuan Wang, Gregory A. Dasch, Claudio J. Struchiner, Greg Madey, Linda I. Hannick, Shelby Bidwell, Vinita Joardar, Elisabet Caler, Renfu Shao, Stephen C. Barker, Stephen Cameron, Robert V. Bruggner, Allison Regier, Justin Johnson, Lakshmi Viswanathan, Terry R. Utterback, Granger G. Sutton, Daniel Lawson, Robert M. Waterhouse, J. Craig Venter, Robert L. Strausberg, May R. Berenbaum, Frank H. Collins, Evgeny M. Zdobnov, and Barry R. Pittendrigh
  1. aJ. Craig Venter Institute, Rockville, MD 20850;
  2. bDepartment of Entomology, University of Illinois, Urbana, IL 61801;
  3. cSchool of Biological Sciences, Bangor University, Bangor, Wales LL57 2UW, United Kingdom;
  4. dSchool of Biological Sciences, University of Reading, Reading RG6 6AS, United Kingdom;
  5. eDepartment of Veterinary and Animal Science, University of Massachusetts, Amherst, MA 01003;
  6. fDepartment of Agricultural Biotechnology, Seoul National University, Seoul, South Korea;
  7. gEck Institute for Global Health, University of Notre Dame, Notre Dame, IN 46556;
  8. hDepartment of Computer Science and Engineering, University of Notre Dame, Notre Dame, IN 46556;
  9. iDepartment of Biology and Biochemistry, University of Houston, Houston, TX 77204;
  10. jDepartment of Genetic Medicine and Development, University of Geneva Medical School, 1211 Geneva, Switzerland;
  11. kSwiss Institute of Bioinformatics, 1211 Geneva, Switzerland;
  12. lDepartment of Animal Science, Texas A&M University, College Station, TX 77843;
  13. mDepartment of Entomology, Purdue University, West Lafayette, IN 47907;
  14. nCentre National de la Recherche Scientifique, Centre Neurosciences Intégratives et Cognitives, University of Bordeaux, 33405 Talence Cedex, France;
  15. oServicio de Hematoloxía, Complexo Hospitalario Universitario de Santiago de Compostela, 15706 Santiago de Compostela, Spain;
  16. pLaboratory of Malaria and Vector Research, National Institutes of Health, Bethesda, MD 20892-8132;
  17. qDepartament de Genètica, Universitat de Barcelona, 08028 Barcelona, Spain;
  18. rDepartment of Entomology, Texas A&M University, College Station, TX 77843;
  19. sDepartment of Biological Sciences, Wayne State University, Detroit, MI 48202;
  20. tServicio de Anatomía Patolóxica, Complexo Hospitalario Universitario de Santiago de Compostela, 15706 Santiago de Compostela, Spain;
  21. uUnité des Rickettsies, 13385 Marseille Cedex 05, France;
  22. vFlorida Museum of Natural History, University of Florida, Gainesville, FL 32611;
  23. wDivision of Biology and Department of Entomology, Kansas State University, Manhattan, KS 66502;
  24. xDepartment of Entomology, Ohio Agriculture Research and Development Center/Ohio State University, Wooster, OH 44691;
  25. yDepartment of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556;
  26. zDepartment of Crop Sciences, Urbana, IL 61801;
  27. aaChung Hwa College of Medical Technology, Jen-Te Hsiang, Tainan 700, Taiwan;
  28. bbCenters for Disease Control and Prevention, Atlanta, GA 30333;
  29. ccEscola Nacional de Saúde Pública Sergio Arouca/Fundação Oswaldo Cruz and Instituto de Medicina Social Universidade do Estado do Rio de Janeiro, 4365 Rio de Janeiro, Brazil;
  30. ddSchool of Chemistry and Molecular Biosciences, University of Queensland, St. Lucia, Brisbane, Queensland 4072, Australia;
  31. eeAustralian National Insect Collection and Commonwealth Scientific and Industrial Research Organization Entomology, Canberra ACT 2601, Australia;
  32. ffEuropean Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SD, United Kingdom; and
  33. ggImperial College London, London SW7 2AZ, United Kingdom.

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PNAS first published June 21, 2010; https://doi.org/10.1073/pnas.1003379107
Ewen F. Kirkness
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Brian J. Haas
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Weilin Sun
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John M. Clark
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Barry R. Pittendrigh
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  • For correspondence: pittendr@illinois.edu
  1. Contributed by May R. Berenbaum, April 14, 2010 (sent for review February 10, 2010)

  2. ↵ 1E.F.K., E.M.Z., and B.R.P. contributed equally to this work.

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Abstract

As an obligatory parasite of humans, the body louse (Pediculus humanus humanus) is an important vector for human diseases, including epidemic typhus, relapsing fever, and trench fever. Here, we present genome sequences of the body louse and its primary bacterial endosymbiont Candidatus Riesia pediculicola. The body louse has the smallest known insect genome, spanning 108 Mb. Despite its status as an obligate parasite, it retains a remarkably complete basal insect repertoire of 10,773 protein-coding genes and 57 microRNAs. Representing hemimetabolous insects, the genome of the body louse thus provides a reference for studies of holometabolous insects. Compared with other insect genomes, the body louse genome contains significantly fewer genes associated with environmental sensing and response, including odorant and gustatory receptors and detoxifying enzymes. The unique architecture of the 18 minicircular mitochondrial chromosomes of the body louse may be linked to the loss of the gene encoding the mitochondrial single-stranded DNA binding protein. The genome of the obligatory louse endosymbiont Candidatus Riesia pediculicola encodes less than 600 genes on a short, linear chromosome and a circular plasmid. The plasmid harbors a unique arrangement of genes required for the synthesis of pantothenate, an essential vitamin deficient in the louse diet. The human body louse, its primary endosymbiont, and the bacterial pathogens that it vectors all possess genomes reduced in size compared with their free-living close relatives. Thus, the body louse genome project offers unique information and tools to use in advancing understanding of coevolution among vectors, symbionts, and pathogens.

  • ectoparasite
  • comparative genomics
  • coevolution

Footnotes

  • 5To whom correspondence should be addressed. E-mail: pittendr{at}illinois.edu.
  • Author contributions: E.F.K., B.J.H., J.M.C., H.M.R., R.C.K., E.E., C.G.E., D. Graur, C.A.H., B.W., J.M.C.T., J.M.C.R., J.R., J.S.J., J.T.R., M.T., D.L.R., O.M., V.M.M., J.M.M., J.R.-S., J.P.V., M.A., J.M.A., K.S.Y., J.P.S., M.F.U., S. Christley, N.F.L., G.A.D., C.J.S., G.M., S. Cameron, A.R., G.G.S., J.C.V., R.L.S., F.H.C., E.M.Z., and B.R.P. designed research; B.J.H., W.S., J.M.C., S.H.L., R.C.K., E.E., D. Gerlach, E.V.K., C.G.E., D. Graur, C.A.H., J.A.V., B.W., J.M.C.R., J.R., J.S.J., J.T.R., A.P., Y.T., M.T., D.R., D.L.R., E.K., O.M., H.-M.L., J.M.M., R.J., J.R.-S., J.P.V., D.A.-P., F.G.V., M.A., S.G.-R., J.M.A., K.S.Y., J.P.S., M.F.U., S. Christley, M.J.S., N.W., C.J.S., R.S., S.C.B., A.R., J.J., L.V., T.R.U., D.L., R.M.W., M.R.B., E.M.Z., and B.R.P. performed research; J.M.C., R.C.K., E.E., C.G.E., D. Graur, C.A.H., J.M.C.T., J.S.J., J.T.R., M.T., J.M.M., J.R.-S., J.M.A., K.S.Y., J.P.S., M.F.U., S. Christley, L.I.H., V.J., E.C., R.S., S.C.B., R.V.B., L.V., R.M.W., and E.M.Z., contributed new reagents or analytic tools; E.F.K., W.S., H.R.B., M.A.P., S.H.L., H.M.R., R.C.K., D. Gerlach, E.V.K., J.A.V., B.W., J.M.C.T., J.M.C.R., J.R., A.P., Y.T., M.T., D.L.R., H.-M.L., R.J., J.R.-S., D.A.-P., F.G.V., M.A., S.G.-R., K.S.Y., J.P.S., M.F.U., S. Christley, M.J.S., N.W., G.A.D., C.J.S., L.I.H., S.C.B., V.J., E.C., R.S., S. Cameron, R.V.B., A.R., J.J., D.L., R.M.W., M.R.B., F.H.C., E.M.Z., and B.R.P. analyzed data; and E.F.K., B.J.H., W.S., H.R.B., M.A.P., S.H.L., H.M.R., R.C.K., B.W., J.M.C.T., J.R., A.P., Y.T., M.T., D.R., D.L.R., O.M., R.J., D.A.-P., F.G.V., M.A., S.G.-R., J.M.A., K.S.Y., J.P.S., M.F.U., S. Christley, G.M., S. Cameron, A.R., R.M.W., M.R.B., F.H.C., E.M.Z., and B.R.P. wrote the paper.

  • The authors declare no conflict of interest.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AAZO00000000, NC_014109, and NC_013962).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1003379107/-/DCSupplemental.

    Freely available online through the PNAS open access option.

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    Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle
    Ewen F. Kirkness, Brian J. Haas, Weilin Sun, Henk R. Braig, M. Alejandra Perotti, John M. Clark, Si Hyeock Lee, Hugh M. Robertson, Ryan C. Kennedy, Eran Elhaik, Daniel Gerlach, Evgenia V. Kriventseva, Christine G. Elsik, Dan Graur, Catherine A. Hill, Jan A. Veenstra, Brian Walenz, José Manuel C. Tubío, José M. C. Ribeiro, Julio Rozas, J. Spencer Johnston, Justin T. Reese, Aleksandar Popadic, Marta Tojo, Didier Raoult, David L. Reed, Yoshinori Tomoyasu, Emily Krause, Omprakash Mittapalli, Venu M. Margam, Hong-Mei Li, Jason M. Meyer, Reed M. Johnson, Jeanne Romero-Severson, Janice Pagel VanZee, David Alvarez-Ponce, Filipe G. Vieira, Montserrat Aguadé, Sara Guirao-Rico, Juan M. Anzola, Kyong S. Yoon, Joseph P. Strycharz, Maria F. Unger, Scott Christley, Neil F. Lobo, Manfredo J. Seufferheld, NaiKuan Wang, Gregory A. Dasch, Claudio J. Struchiner, Greg Madey, Linda I. Hannick, Shelby Bidwell, Vinita Joardar, Elisabet Caler, Renfu Shao, Stephen C. Barker, Stephen Cameron, Robert V. Bruggner, Allison Regier, Justin Johnson, Lakshmi Viswanathan, Terry R. Utterback, Granger G. Sutton, Daniel Lawson, Robert M. Waterhouse, J. Craig Venter, Robert L. Strausberg, May R. Berenbaum, Frank H. Collins, Evgeny M. Zdobnov, Barry R. Pittendrigh
    Proceedings of the National Academy of Sciences Jun 2010, 201003379; DOI: 10.1073/pnas.1003379107

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    Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle
    Ewen F. Kirkness, Brian J. Haas, Weilin Sun, Henk R. Braig, M. Alejandra Perotti, John M. Clark, Si Hyeock Lee, Hugh M. Robertson, Ryan C. Kennedy, Eran Elhaik, Daniel Gerlach, Evgenia V. Kriventseva, Christine G. Elsik, Dan Graur, Catherine A. Hill, Jan A. Veenstra, Brian Walenz, José Manuel C. Tubío, José M. C. Ribeiro, Julio Rozas, J. Spencer Johnston, Justin T. Reese, Aleksandar Popadic, Marta Tojo, Didier Raoult, David L. Reed, Yoshinori Tomoyasu, Emily Krause, Omprakash Mittapalli, Venu M. Margam, Hong-Mei Li, Jason M. Meyer, Reed M. Johnson, Jeanne Romero-Severson, Janice Pagel VanZee, David Alvarez-Ponce, Filipe G. Vieira, Montserrat Aguadé, Sara Guirao-Rico, Juan M. Anzola, Kyong S. Yoon, Joseph P. Strycharz, Maria F. Unger, Scott Christley, Neil F. Lobo, Manfredo J. Seufferheld, NaiKuan Wang, Gregory A. Dasch, Claudio J. Struchiner, Greg Madey, Linda I. Hannick, Shelby Bidwell, Vinita Joardar, Elisabet Caler, Renfu Shao, Stephen C. Barker, Stephen Cameron, Robert V. Bruggner, Allison Regier, Justin Johnson, Lakshmi Viswanathan, Terry R. Utterback, Granger G. Sutton, Daniel Lawson, Robert M. Waterhouse, J. Craig Venter, Robert L. Strausberg, May R. Berenbaum, Frank H. Collins, Evgeny M. Zdobnov, Barry R. Pittendrigh
    Proceedings of the National Academy of Sciences Jun 2010, 201003379; DOI: 10.1073/pnas.1003379107
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