Agriculture News

February 2, 2016  

Bedbug genome uncovers biology of a pest on the rebound

Scharf bedbug

Bedbugs can grow up to a quarter inch long and have piercing-sucking mouthparts. Their resurgence in the U.S. has reached "almost a crisis condition," Purdue entomologists said. (Purdue University photo/Andrew Nuss)
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WEST LAFAYETTE, Ind. - Purdue University researchers participated in a multi-institute project that sequenced the genome of the common bedbug, a blood-sucking insect that has reemerged globally as a hardy pest capable of withstanding most major classes of insecticides.

The genome of Cimex lectularius uncovers the genetic underpinning of bedbugs' unique biology and offers new targets for controlling them.

Purdue entomologists Ameya Gondhalekar and Michael Scharf contributed to the international effort by annotating the bugs' antioxidant genes, which detoxify the blood they ingest and likely play a role in disarming certain types of insecticides.

"Bedbugs were the ignored pests for many decades, but their sudden prevalence has sparked interest in developing better bedbug control measures and knowing more about their biology," said Gondhalekar, an assistant professor of entomology. "The genome provides a much-needed platform for answering these questions at a deeper level."

Bedbugs have plagued humans for at least 3,000 years, emerging at night to feed on blood, their sole source of nutrition and water. Widespread use of insecticides in homes after World War II curtailed their numbers dramatically, but over the past two decades, the bedbug has rebounded from near eradication in many regions to extraordinary levels of infestation on every continent except Antarctica. Infestations in Australia alone have risen 4,500 percent.

The bug's unexpected comeback is likely due to a surge in international travel, the exchange of secondhand goods and the pest's evolution of resistance to many conventional insecticides, said Scharf, the O. Wayne Rollins/Orkin Chair in Molecular Physiology and Entomology.

"Nobody was ready for this," he said. "It's reached almost a crisis condition. All big cities in the U.S. are experiencing problems. Our culture had forgotten about bedbugs, and two generations of entomologists haven't had to deal with them."

The genome shows that bedbugs have developed multiple ways of resisting insecticides. Their armor-like outer cuticle sports barriers and detoxification genes that help prevent insecticides from penetrating. Many bedbugs have also evolved new forms of sodium channels, gates in the nervous system that insecticides such as pyrethroids are designed to target and disrupt. The bugs might also detoxify ingested pesticides using the same robust antioxidant enzyme system they use to detoxify blood, the researchers said.

The genome indicated substantial inbreeding among bedbugs, suggesting that genetic resistance to pesticides can spread across populations.

Many of the bedbug genes associated with pesticide resistance have similar forms in other insects such as mosquitoes and fruit flies, but Scharf and Gondhalekar pinpointed antioxidant genes that appear to be unique to bedbugs, offering possible targets for genetic control measures.

Other factors that make bedbugs tough to control are their abilities to survive for months without a blood meal, easily hitchhike on clothes and luggage, feed stealthily, and stow away in furniture and mattresses. Many insecticides can only be applied to cracks, crevices and baseboards, allowing the bugs to hide during spraying and emerge unscathed later.

"It only takes one pregnant bedbug to jumpstart an infestation of a whole building," Scharf said.

Adult bedbugs can grow up to a quarter inch long and are flat, reddish-brown insects that resemble oversized versions of their sister species, the pea aphid. They use piercing-sucking mouthparts to penetrate human skin and slurp up a blood meal, typically leaving behind an itchy, red welt.

Severity of reactions to bedbug bites can vary widely, and the genome provides researchers with molecular resources to investigate whether proteins produced by bedbugs can cause allergies.

Though the bugs do not transmit disease, scratching bedbug bites can result in secondary infections, and infestations can exert a psychological toll, the researchers said.

People in infested homes can suffer from stress, paranoia, poor quality of sleep, insomnia and depression.

"Once you have bedbugs, everything changes," Gondhalekar said. "You devote all your attention to getting rid of them."

Previous research by Purdue entomologist Timothy Gibb showed that even people who mistakenly thought their homes were infested showed an increase in depression and distanced themselves from others.

"People feel vulnerable," Scharf said. "You're being fed upon by something that drinks your blood while you're sleeping."

The genome also revealed that bedbugs have a significantly lower number of chemosensory genes compared with many other insects, possibly due to the bedbugs' host specificity. They have inherited genes from symbiotic bacteria that provide essential nutrients lacking in blood. Bedbugs also have a large number of genes that code for resilin, which gives their cuticle elasticity. This adaptation likely helps female bedbugs recover after traumatic insemination, a mating process in which the male stabs the female's abdomen with dagger-like genitalia.

The researchers said that pesticide companies could leverage these genomic resources to screen the effectiveness of available chemicals, lowering the cost of getting new insecticides to market.

"Fortunately, we've now got the genome early in the game," Scharf said. "Having this knowledge now might enable us to prevent bedbugs from becoming pests at the level of German cockroaches or disease-transmitting mosquitoes."

The paper was published in Nature Communications on Tuesday (Feb. 2) and is available at http://dx.doi.org/10.1038/ncomms10165.

Funding for the project was provided by the National Institutes of Health, NIH's National Human Genome Research Institute, the Blanton J. Whitmore Endowment, Housing and Urban Development, the National Science Foundation, the Alfred P. Sloan Foundation, the Royal Society of New Zealand Marsden Fast Start Grant, the Fralin Life Sciences Institutes and Virginia Agriculture Experimental Station, the European Research Council, the Deutsche Forschungsgemeinschaft, Biotechnology and Biological Sciences Research Council, the University of Cincinnati Faculty Development Research Grant, the Ohio Supercomputer Center Research Allocation, the Marie Curie International Outgoing Fellowship, the Swiss National Science Foundation. The 5,000 arthropod genomes initiative also assisted in the genome sequencing. 

Writer: Natalie van Hoose, 765-496-2050, nvanhoos@purdue.edu 

Sources: Michael Scharf, 765-496-6710, mscharf@purdue.edu

Ameya Gondhalekar, 765-494-3839, ameyag@purdue.edu 


ABSTRACT

Unique Features of a Global Human Ectoparasite Identified Through Sequencing of the Bed Bug Genome

Joshua B. Benoit 1; Zach N. Adelman 2; Klaus Reinhardt 3; Amanda Dolan 4; Monica Poelchau 5; Emily C. Jennings 1; Elise M. Szuter 1; Richard W. Hagan 1; Hemant Gujar 6; Jayendra Nath Shukla 6; Fang Zhu 6,7; M. Mohan 8; David R. Nelson 9; Andrew J. Rosendale 1; Christian Derst 10; Valentina Resnik 11; Sebastian Wernig 11; Pamela Menegazzi 12; Christian Wegener 12; Nicolai Peschel 12; Jacob M. Hendershot 1; Wolfgang Blenau 10; Reinhard Predel 10; Paul R. Johnston 13; Panagiotis Ioannidis 15; Robert M. Waterhouse 15,16; Ralf Nauen 17; Corinna Schorn 17; Mark-Christoph Ott 17; Frank Maiwald 17; J. Spencer Johnston 14; Ameya D. Gondhalekar 18; Michael E. Scharf 18; Brittany F. Peterson 18; Kapil R. Raje18; Benjamin A. Hottel 19; David Armisen 20; Antonin Jean Johan Crumiere 20; Peter Nagui Refki 20; Maria Emilia Santos 20; Essia Sghaier 20; 
Severine Viala 20; Abderrahman Khila 20; Seung-Joon Ahn 21; Christopher Childers 5; Chien-Yueh Lee 5,22; Han Lin 5,22; Daniel S.T. Hughes 23; Elizabeth J. Duncan 24; Shwetha C. Murali 23; Jiaxin Qu 23; Shannon Dugan 23; Sandra L. Lee 23; Hsu Chao 23; Huyen Dinh 23; Yi Han 23; Harshavardhan Doddapaneni 23; Kim C. Worley 23; Donna M. Muzny 23; David Wheeler 25; Kristen A. Panfilio 26; Iris M. Vargas Jentzsch 26; Edward L. Vargo 14; Warren Booth 27; Markus Friedrich 28; Matthew T. Weirauch 29; Michelle A.E. Anderson 2; Jeffery W. Jones 28; 
Omprakash Mittapalli 30; Chaoyang Zhao 30; Jing-Jiang Zhou 31; Jay D. Evans 32; Geoffrey M. Attardo 33; Hugh M. Robertson 34; Evgeny M. Zdobnov 15; Jose M.C. Ribeiro 35; Richard A. Gibbs 23; John H. Werren 4; Subba R. Palli 6; Coby Schal 36 & Stephen Richards 23

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 fur Bienenkunde (Polytechnische Gesellschaft), Goethe University Frankfurt, Oberursel 61440, Germany

12 Department of Neurobiology and Genetics, Theodor-Boveri-Institute, Biocenter, University of Wurzburg, Wurzburg 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 Ge ́nomique Fonctionnelle de Lyon (IGFL), Ecole Normale Supe ́rieure de Lyon, UMR5242-CNRS, Lyon 69007, France

21 Department of Entomology, Max Plank 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 Correspondence and requests for materials should be addressed to J.B.B. (email: joshua.benoit@uc.edu) or to S.R. (email: stephenr@bcm.edu).

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 (650Mb) 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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