Abstract
Cimex lectularius, known as the common bed bug, is a widespread hematophagous human ectoparasite and urban pest that is not known to be a vector of any human infectious disease agents. However, few studies in the era of molecular biology have profiled the microorganisms harbored by field populations of bed bugs. The objective of this study was to examine the viruses present in a large sampling of common bed bugs and related bat bugs (Cimex pipistrelle). RNA sequencing was undertaken on an international sampling of > 500 field-collected bugs, and multiple workflows were used to assemble contigs and query these against reference nucleotide databases to identify viral genomes. Shuangao bed bug virus 2, an uncharacterized rhabdovirus previously discovered in Cimex hemipterus from China, was found in several bed bug pools from the USA and Europe, as well as in C. pipistrelle, suggesting that this virus is common among bed bug populations. In addition, Shuangao bed bug virus 1 was detected in a bed bug pool from China, and sequences matching Enterobacteria phage P7 were found in all bed bug pools, indicating the ubiquitous presence of phage-derived elements in the genome of the bed bug or its enterobacterial symbiont. However, viral diversity was low in bed bugs in our study, as no other viral genomes were detected with significant coverage. These results provide evidence against frequent virus infection in bed bugs. Nonetheless, our investigation had several important limitations, and additional studies should be conducted to better understand the prevalence and composition of viruses in bed bugs. Most notably, our study largely focused on insects from urban areas in industrialized nations, thus likely missing infrequent virus infections and those that could occur in rural or tropical environments or developing nations.
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Data availability
Raw sequencing reads are publicly available for additional mining and analysis. These can be accessed from the NCBI SRA under BioProject ID: PRJNA972449.
References
Adelman ZN, Miller DM, Myles KM (2013) Bed bugs and infectious disease: a case for the arboviruses. PLoS Pathog 9(8):e1003462
Afgan E, Baker D, Batut B, van den Beek M, Bouvier D, Cech M, Chilton J, Clements D, Coraor N, Grüning BA, Guerler A, Hillman-Jackson J, Hiltemann S, Jalili V, Rasche H, Soranzo N, Goecks J, Taylor J, Nekrutenko A, Blankenberg D (2018) The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res 46(W1):W537–W544
Antipov D, Raiko M, Lapidus A, Pevzner PA (2020) Metaviral SPAdes: assembly of viruses from metagenomic data. Bioinformatics 36(14):4126–4129
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421
CDC Division of Vector-Borne Diseases (DVBD)- Arbovirus catalog. https://wwwn.cdc.gov/Arbocat/Default.aspx. Accessed 26 Apr 2023
Cock PJ, Chilton JM, Grüning B, Johnson JE, Soranzo N (2015) NCBI BLAST+ integrated into Galaxy. Gigascience 4:39
Delaunay P, Blanc V, Del Giudice P, Levy-Bencheton A, Chosidow O, Marty P, Brouqui P (2011) Bedbugs and infectious diseases. Clin Infect Dis 52(2):200–210
Doggett SL, Dwyer DE, Peñas PF, Russell RC (2012) Bed bugs: clinical relevance and control options. Clin Microbiol Rev 25(1):164–192
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652
Harlan HJ, Faulde MK, Baumann GJ (2008) Bed bugs. Public health significance of urban pests. Editors: Bonnefoy X, Kampen H, Sweeney K. World Health Organization. 131–151
Hatcher EL, Zhdanov SA, Bao Y, Blinkova O, Nawrocki EP, Ostapchuck Y, Schäffer AA, Brister JR (2017) Virus Variation Resource - improved response to emergent viral outbreaks. Nucleic Acids Res 45(D1):D482–D490
Hayes RO, Francy DB, Lazuick JS, Smith GC, Gibbs EPJ (1977) Role of the cliff swallow bug (Oeciacus vicarius) in the natural cycle of a western equine encephalitis-related alphavirus. J Med Entomol 14:257–262
Ho D, Lai O, Glick S, Jagdeo J (2016) Lack of evidence that bedbugs transmit pathogens to humans. J Am Acad Dermatol 74(6):1261
Kalantar KL, Carvalho T, de Bourcy CFA, Dimitrov B, Dingle G, Egger R, Han J, Holmes OB, Juan YF, King R, Kislyuk A, Lin MF, Mariano M, Morse T, Reynoso LV, Cruz DR, Sheu J, Tang J, Wang J, Zhang MA, Zhong E, Ahyong V, Lay S, Chea S, Bohl JA, Manning JE, Tato CM, DeRisi JL (2020) IDseq-An open source cloud-based pipeline and analysis service for metagenomic pathogen detection and monitoring. Gigascience 9(10):giaa111. https://doi.org/10.1093/gigascience/giaa111
Kim D, Paggi JM, Park C, Bennett C, Salzberg SL (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol 37(8):907–915
Li CX, Shi M, Tian JH, Lin XD, Kang YJ, Chen LJ, Qin XC, Xu J, Holmes EC, Zhang YZ (2015) Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. Elife 4:e05378
Ling J, Persson Vinnersten T, Hesson JC, Bohlin J, Roligheten E, Holmes EC, Pettersson JH (2020) Identification of hepatitis C virus in the common bed bug - a potential, but uncommon route for HCV infection? Emerg Microbes Infect 9(1):1429–1431
Lai O, Ho D, Glick S, Jagdeo J (2016) Bed bugs and possible transmission of human pathogens: a systematic review. Arch Dermatol Res 308:531–538
Ndiaye EHI, Diatta G, Diarra AZ, Berenger JM, Bassene H, Mediannikov O, Bouganali C, Sokhna C, Parola P (2022) Morphological, molecular and MALDI-TOF MS identification of bedbugs and associated Wolbachia species in rural Senegal. J Med Entomol 59(3):1019–1032
Peta V, Tantely LM, Potts R, Girod R, Pietri JE (2022) A Francisella tularensis-like bacterium in tropical bed bugs from Madagascar. Vector Borne Zoonotic Dis 22(1):58–61
Pietri JE (2020) Case not closed: arguments for new studies of the interactions between bed bugs and human pathogens. Am J Trop Med Hyg 103(2):619–624
Potts R, Peta V, Agany DDM, Gnimpieba EZ, Cooper R, Wang C, Pietri JE (2021) Molecular analysis of the blood meals and bacterial communities of bed bugs (Cimex lectularius L.) to assess interactions with alternative hosts. Parasitol Res 120(4):1209–1217
Rush WA, Francy DB, Smith GC, Cropp CB (1980) Transmission of an arbovirus by a member of the family Cimicidae. Ann Entomol Soc Am 73:315–318
Sakamoto JM, Rasgon J (2006) Endosymbiotic bacteria of bed bugs: evolution, ecology and genetics. Am Entomol 52:119–122
Sevestre J, Lemrabott MAO, Bérenger JM, Zan Diarra A, Boukhary AOMS, Parola P (2023) Detection of arthropod-borne bacteria and assessment of MALDI-TOF MS for the identification of field-collected immature bed bugs from Mauritania. Insects 14(1):69
Sheele JM, Mallipeddi N, Coppolino K, Chetverikova M, Mothkur S, Caiola C (2016) FMC Verifi traps are not effective for quantifying the burden of bed bugs in an emergency department. Am J Infect Control 44(9):1078–1080
Sheele JM, Barrett E, Farhan O, Morris N (2017a) Analysis of bed bug (Cimex lectularius) introductions into an academic medical center. Infect Control Hosp Epidemiol 38(5):623–624
Sheele JM, Barrett E, Dash D, Ridge GE (2017b) Analysis of the life stages of Cimex lectularius captured within a medical centre suggests that the true numbers of bed bug introductions are under-reported. J Hosp Infect 97(3):310–312
Sheele JM, Gaines S, Maurer N, Coppolino K, Li JS, Pound A, Luk JH, Mandac E (2017c) A survey of patients with bed bugs in the emergency department. Am J Emerg Med 35(5):697–698
Sheele JM, Crandall CJ, Chang BF, Arko BL, Dunn CT, Negrete A (2019a) Characteristics of bed bug infested patients in the emergency department. Emerg Med Int 2019:8721829
Sheele JM, Crandall CJ, Chang BF, Arko BL, Dunn CT, Negrete A (2019b) Risk factors for bed bugs among urban emergency department patients. J Community Health 31:1–8
Stanojević M, Li K, Stamenković G, Ilić B, Paunović M, Pešić B, Maslovara IĐ, Šiljić M, Ćirković V, Zhang Y (2020) Depicting the RNA virome of hematophagous arthropods from Belgrade, Serbia. Viruses 12(9):975
Totten V, Charbonneau H, Hoch W, Shah S, Sheele JM (2016) The cost of decontaminating an ED after finding a bed bug: results from a single academic medical center. Am J Emerg Med 34(3):649
Williams JE, Imlarp S, Top FH Jr, Cavanaugh DC, Russell PK (1976) Kaeng Khoi virus from naturally infected bedbugs (cimicidae) and immature free-tailed bats. Bull World Health Organ 53(4):365
Xu Z, Feng Y, Chen X, Shi M, Fu S, Yang W, Liu WJ, Gao GF, Liang G (2022) Virome of bat-infesting arthropods: highly divergent viruses in different vectors. J Virol 96(4):e0146421
Acknowledgements
We thank the following individuals and organizations for providing samples, laboratory assistance, or communications regarding sequencing: Logan Pest, General Pest Control, Hoban Pest Control, Patton Pest Control, Clark Pest Control, Southwest Exterminating, Charlie Masters, Mike Lipsett, Jason Temple, Rick DeDonato, Steve Kmetz, Carl Easter, Jeff Satzman, Luis Agurto, Pat Zickler, Alan Feuer, John Gedeon, Changlu Wang, Yijuan Xu, Jean-Michel Berenger, Maureen Laroche, Richard Naylor, E. Ricky Chan, Gale Ridge, Andrew Young, John Gibson, Richard Cooper, Jeff White, Clarise Starr, and Terry Humphrey.
Funding
The study was supported by an internal UHCMC Department of Emergency Medicine Ford Geriatric Emergency Medicine award to JMS and by a US HUD Office of Lead Hazard Control and Healthy Homes, Healthy Homes Technical Studies grant (SDHHU0074-22) to JEP.
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JS: investigation, conceptualization, methodology, validation, supervision, funding acquisition, resources, writing—original draft, writing—review and editing. VP: formal analysis. writing—original draft, writing—review and editing. AM: conceptualization, methodology, resources. OB: resources. DC: resources. SE: conceptualization, methodology. TM: conceptualization, methodology, resources. JP: investigation, conceptualization, methodology, validation, supervision, funding acquisition, writing—original draft, writing—review and editing.
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Sheele, J.M., Peta, V., Miron, A. et al. A metatranscriptomic evaluation of viruses in field-collected bed bugs. Parasitol Res 123, 4 (2024). https://doi.org/10.1007/s00436-023-08049-1
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DOI: https://doi.org/10.1007/s00436-023-08049-1