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

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      a , 1 , 2 , 3 , 4 , 5 , 1 , 1 , 1 , 6 , 6 , 6 , 7 , 8 , 9 , 1 , 10 , 11 , 11 , 12 , 12 , 12 , 1 , 10 , 10 , 13 , 15 , 15 , 16 , 17 , 17 , 17 , 17 , 14 , 18 , 18 , 18 , 18 , 19 , 20 , 20 , 20 , 20 , 20 , 20 , 20 , 21 , 5 , 5 , 22 , 5 , 22 , 23 , 24 , 23 , 23 , 23 , 23 , 23 , 23 , 23 , 23 , 23 , 23 , 25 , 26 , 26 , 14 , 27 , 28 , 29 , 2 , 28 , 30 , 30 , 31 , 32 , 33 , 34 , 15 , 35 , 23 , 4 , 6 , 36 , b , 23
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          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.

          Abstract

          The bed bug, Cimex lectularius, is a ubiquitous human ectoparasite with global distribution. Here, the authors sequence the genome of the bed bug and identify reductions in chemosensory genes, expansion of genes associated with blood digestion and genes linked to pesticide resistance.

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          Most cited references61

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          Wolbachia: master manipulators of invertebrate biology.

          Wolbachia are common intracellular bacteria that are found in arthropods and nematodes. These alphaproteobacteria endosymbionts are transmitted vertically through host eggs and alter host biology in diverse ways, including the induction of reproductive manipulations, such as feminization, parthenogenesis, male killing and sperm-egg incompatibility. They can also move horizontally across species boundaries, resulting in a widespread and global distribution in diverse invertebrate hosts. Here, we review the basic biology of Wolbachia, with emphasis on recent advances in our understanding of these fascinating endosymbionts.
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            Wolbachia as a bacteriocyte-associated nutritional mutualist.

            Many insects are dependent on bacterial symbionts that provide essential nutrients (ex. aphid-Buchnera and tsetse-Wiglesworthia associations), wherein the symbionts are harbored in specific cells called bacteriocytes that constitute a symbiotic organ bacteriome. Facultative and parasitic bacterial symbionts like Wolbachia have been regarded as evolutionarily distinct from such obligate nutritional mutualists. However, we discovered that, in the bedbug Cimex lectularius, Wolbachia resides in a bacteriome and appears to be an obligate nutritional mutualist. Two bacterial symbionts, a Wolbachia strain and an unnamed gamma-proteobacterium, were identified from different strains of the bedbug. The Wolbachia symbiont was detected from all of the insects examined whereas the gamma-proteobacterium was found in a part of them. The Wolbachia symbiont was specifically localized in the bacteriomes and vertically transmitted via the somatic stem cell niche of germalia to oocytes, infecting the incipient symbiotic organ at an early stage of the embryogenesis. Elimination of the Wolbachia symbiont resulted in retarded growth and sterility of the host insect. These deficiencies were rescued by oral supplementation of B vitamins, confirming the essential nutritional role of the symbiont for the host. The estimated genome size of the Wolbachia symbiont was around 1.3 Mb, which was almost equivalent to the genome sizes of parasitic Wolbachia strains of other insects. These results indicate that bacteriocyte-associated nutritional mutualism can evolve from facultative and prevalent microbial associates like Wolbachia, highlighting a previously unknown aspect of the parasitism-mutualism evolutionary continuum.
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              Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes.

              Although common among bacteria, lateral gene transfer-the movement of genes between distantly related organisms-is thought to occur only rarely between bacteria and multicellular eukaryotes. However, the presence of endosymbionts, such as Wolbachia pipientis, within some eukaryotic germlines may facilitate bacterial gene transfers to eukaryotic host genomes. We therefore examined host genomes for evidence of gene transfer events from Wolbachia bacteria to their hosts. We found and confirmed transfers into the genomes of four insect and four nematode species that range from nearly the entire Wolbachia genome (>1 megabase) to short (<500 base pairs) insertions. Potential Wolbachia-to-host transfers were also detected computationally in three additional sequenced insect genomes. We also show that some of these inserted Wolbachia genes are transcribed within eukaryotic cells lacking endosymbionts. Therefore, heritable lateral gene transfer occurs into eukaryotic hosts from their prokaryote symbionts, potentially providing a mechanism for acquisition of new genes and functions.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                02 February 2016
                2016
                : 7
                : 10165
                Affiliations
                [1 ]Department of Biological Sciences, University of Cincinnati , Cincinnati, Ohio 45221, USA
                [2 ]Fralin Life Science Institute and Department of Entomology, Virginia Tech , Blacksburg, Virginia 24061, USA
                [3 ]Department of Biology, Applied Zoology, Technische Universitaet Dresden , Dresden 01062, Germany
                [4 ]Department of Biology, University of Rochester , Rochester, New York 14627, USA
                [5 ]National Agricultural Library , Beltsville, Maryland 20705, USA
                [6 ]Department of Entomology, University of Kentucky , Lexington, Kentucky 40546, USA
                [7 ]Department of Entomology, Washington State University , Pullman, Washington 99164, USA
                [8 ]ICAR-National Bureau of Agricultural Insect Resources, Indian Council of Agricultural Research , Bengaluru 560024, India
                [9 ]Department of Microbiology, Immunology, and Biochemistry, University of Tennessee Health Sciences Center , Memphis, Tennessee 38163, USA
                [10 ]Cologne Biocenter and Zoological Institute, University of Cologne , Cologne 50674, Germany
                [11 ]Institut für Bienenkunde (Polytechnische Gesellschaft), Goethe University Frankfurt , Oberursel 61440, Germany
                [12 ]Department of Neurobiology and Genetics, Theodor-Boveri-Institute, Biocenter, University of Würzburg , Würzburg 97074, Germany
                [13 ]Department of Evolutionary Biology, Institute of Biology, Freie Universitaet , Berlin 14195, Germany
                [14 ]Department of Entomology, Texas A&M University , College Station, Texas 77843, USA
                [15 ]Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva , Geneva 1211, Switzerland
                [16 ]Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology and The Broad Institute of MIT and Harvard , Cambridge, Massachusetts 02139, USA
                [17 ]Pest Control Biology and Research Technologies, Bayer CropScience AG , Monheim 40789, Germany
                [18 ]Department of Entomology, Purdue University , West Lafayette, Indiana 47907, USA
                [19 ]Department of Entomology and Nematology, University of Florida , Gainesville, Florida 32611, USA
                [20 ]Institue de Génomique Fonctionnelle de Lyon (IGFL), Ecole Normale Supérieure de Lyon, UMR5242-CNRS , Lyon 69007, France
                [21 ]Department of Entomology, Max Planck Institute for Chemical Ecology , Jena 07745, Germany
                [22 ]Graduate Institute of Biomedical Electronics and Bioinformatics, National Taiwan University , Taipei 10617, Taiwan
                [23 ]Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine , Houston, Texas 77030, USA
                [24 ]Department of Biochemistry and Genetics Otago, University of Otago , Dunedin 9054, New Zealand
                [25 ]Institute of Fundamental Science, Massey University , Palmerston North 4442, New Zealand
                [26 ]Institute for Developmental Biology, University of Cologne , Cologne 50674, Germany
                [27 ]Department of Biological Sciences, University of Tulsa , Tulsa, Oklahoma 74104, USA
                [28 ]Department of Biological Sciences, Wayne State University , Detroit, Michigan 48202, USA
                [29 ]Center for Autoimmune Genomics and Etiology, Division of Biomedical Informatics, and Division of Developmental Biology, Cincinnati Children's Hospital Medical Center, Department of Pediatrics, College of Medicine, University of Cincinnati , Cincinnati, Ohio 45229, USA
                [30 ]Department of Entomology, The Ohio State University , Wooster, Ohio 44691, USA
                [31 ]Department of Biological Chemistry and Crop Protection, Rothamsted Research, BBSRC Harpenden , Herts AL5 2JQ, UK
                [32 ]United States Department of Agriculture—Agricultural Research Service Bee Research Laboratory , Beltsville, Maryland 20705, USA
                [33 ]Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University , New Haven, Connecticut 06520, USA
                [34 ]Department of Entomology, University of Illinois at Urbana-Champaign , Urbana, Illinois 61801, USA
                [35 ]Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Disease , Bethesda, Maryland 20892, USA
                [36 ]Department of Entomology and W.M. Keck Center for Behavioral Biology, North Carolina State University , Raleigh, North Carolina 27695, USA
                Author notes
                Author information
                http://orcid.org/0000-0003-4481-3567
                http://orcid.org/0000-0002-8651-4488
                http://orcid.org/0000-0003-0939-6745
                http://orcid.org/0000-0003-4199-9052
                http://orcid.org/0000-0002-1253-5550
                http://orcid.org/0000-0002-3446-5098
                http://orcid.org/0000-0003-2355-0702
                http://orcid.org/0000-0002-0036-4651
                Article
                ncomms10165
                10.1038/ncomms10165
                4740739
                26836814
                685f7982-73b7-4bb5-9adf-64c058049641
                Copyright © 2016, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 30 April 2015
                : 10 November 2015
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