skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Mosquito-Borne Viruses and Insect-Specific Viruses Revealed in Field-Collected Mosquitoes by a Monitoring Tool Adapted from a Microbial Detection Array

Abstract

Several mosquito-borne diseases affecting humans are emerging or reemerging in the United States. The early detection of pathogens in mosquito populations is essential to prevent and control the spread of these diseases. Here, we tested the potential applicability of the Lawrence Livermore Microbial Detection Array (LLMDA) to enhance biosurveillance by detecting microbes present in Aedes aegypti, Aedes albopictus, and Culex mosquitoes, which are major vector species globally, including in Texas. The sensitivity and reproducibility of the LLMDA were tested in mosquito samples spiked with different concentrations of dengue virus (DENV), revealing a detection limit of >100 but <1,000 PFU/ml. Additionally, field-collected mosquitoes from Chicago, IL, and College Station, TX, of known infection status (West Nile virus [WNV] and Culex flavivirus [CxFLAV] positive) were tested on the LLMDA to confirm its efficiency. Mosquito field samples of unknown infection status, collected in San Antonio, TX, and the Lower Rio Grande Valley (LRGV), TX, were run on the LLMDA and further confirmed by PCR or quantitative PCR (qPCR). The analysis of the field samples with the LLMDA revealed the presence of cell-fusing agent virus (CFAV) in A. aegypti populations. Wolbachia was also detected in several of the field samples (A. albopictus and Culexmore » spp.) by the LLMDA. Our findings demonstrated that the LLMDA can be used to detect multiple arboviruses of public health importance, including viruses that belong to the Flavivirus, Alphavirus, and Orthobunyavirus genera. Additionally, insect-specific viruses and bacteria were also detected in field-collected mosquitoes. Another strength of this array is its ability to detect multiple viruses in the same mosquito pool, allowing for the detection of cocirculating pathogens in an area and the identification of potential ecological associations between different viruses. Finally, this array can aid in the biosurveillance of mosquito-borne viruses circulating in specific geographical areas.« less

Authors:
 [1];  [2];  [2];  [1];  [2];  [3];  [2];  [1];  [2]
  1. Texas A & M Univ., College Station, TX (United States)
  2. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  3. Texas A & M Univ., San Antonio, TX (United States)
Publication Date:
Research Org.:
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA); National Institutes of Health (NIH)
OSTI Identifier:
1614968
Report Number(s):
LLNL-JRNL-750498
Journal ID: ISSN 0099-2240; 935708
Grant/Contract Number:  
AC52-07NA27344; R21AI128953
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 85; Journal Issue: 19; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats

Martin, Estelle, Borucki, Monica K., Thissen, James, Garcia-Luna, Selene, Hwang, Mona, Wise de Valdez, Megan, Jaing, Crystal J., Hamer, Gabriel L., and Frank, Matthias. Mosquito-Borne Viruses and Insect-Specific Viruses Revealed in Field-Collected Mosquitoes by a Monitoring Tool Adapted from a Microbial Detection Array. United States: N. p., 2019. Web. https://doi.org/10.1128/AEM.01202-19.
Martin, Estelle, Borucki, Monica K., Thissen, James, Garcia-Luna, Selene, Hwang, Mona, Wise de Valdez, Megan, Jaing, Crystal J., Hamer, Gabriel L., & Frank, Matthias. Mosquito-Borne Viruses and Insect-Specific Viruses Revealed in Field-Collected Mosquitoes by a Monitoring Tool Adapted from a Microbial Detection Array. United States. https://doi.org/10.1128/AEM.01202-19
Martin, Estelle, Borucki, Monica K., Thissen, James, Garcia-Luna, Selene, Hwang, Mona, Wise de Valdez, Megan, Jaing, Crystal J., Hamer, Gabriel L., and Frank, Matthias. Fri . "Mosquito-Borne Viruses and Insect-Specific Viruses Revealed in Field-Collected Mosquitoes by a Monitoring Tool Adapted from a Microbial Detection Array". United States. https://doi.org/10.1128/AEM.01202-19. https://www.osti.gov/servlets/purl/1614968.
@article{osti_1614968,
title = {Mosquito-Borne Viruses and Insect-Specific Viruses Revealed in Field-Collected Mosquitoes by a Monitoring Tool Adapted from a Microbial Detection Array},
author = {Martin, Estelle and Borucki, Monica K. and Thissen, James and Garcia-Luna, Selene and Hwang, Mona and Wise de Valdez, Megan and Jaing, Crystal J. and Hamer, Gabriel L. and Frank, Matthias},
abstractNote = {Several mosquito-borne diseases affecting humans are emerging or reemerging in the United States. The early detection of pathogens in mosquito populations is essential to prevent and control the spread of these diseases. Here, we tested the potential applicability of the Lawrence Livermore Microbial Detection Array (LLMDA) to enhance biosurveillance by detecting microbes present in Aedes aegypti, Aedes albopictus, and Culex mosquitoes, which are major vector species globally, including in Texas. The sensitivity and reproducibility of the LLMDA were tested in mosquito samples spiked with different concentrations of dengue virus (DENV), revealing a detection limit of >100 but <1,000 PFU/ml. Additionally, field-collected mosquitoes from Chicago, IL, and College Station, TX, of known infection status (West Nile virus [WNV] and Culex flavivirus [CxFLAV] positive) were tested on the LLMDA to confirm its efficiency. Mosquito field samples of unknown infection status, collected in San Antonio, TX, and the Lower Rio Grande Valley (LRGV), TX, were run on the LLMDA and further confirmed by PCR or quantitative PCR (qPCR). The analysis of the field samples with the LLMDA revealed the presence of cell-fusing agent virus (CFAV) in A. aegypti populations. Wolbachia was also detected in several of the field samples (A. albopictus and Culex spp.) by the LLMDA. Our findings demonstrated that the LLMDA can be used to detect multiple arboviruses of public health importance, including viruses that belong to the Flavivirus, Alphavirus, and Orthobunyavirus genera. Additionally, insect-specific viruses and bacteria were also detected in field-collected mosquitoes. Another strength of this array is its ability to detect multiple viruses in the same mosquito pool, allowing for the detection of cocirculating pathogens in an area and the identification of potential ecological associations between different viruses. Finally, this array can aid in the biosurveillance of mosquito-borne viruses circulating in specific geographical areas.},
doi = {10.1128/AEM.01202-19},
journal = {Applied and Environmental Microbiology},
number = 19,
volume = 85,
place = {United States},
year = {2019},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 2 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Critical review of the vector status of Aedes albopictus
journal, September 2004


Restriction of Zika virus infection and transmission in Aedes aegypti mediated by an insect-specific flavivirus
journal, December 2018

  • Romo, Hannah; Kenney, Joan L.; Blitvich, Bradley J.
  • Emerging Microbes & Infections, Vol. 7, Issue 1
  • DOI: 10.1038/s41426-018-0180-4

Culex Flavivirus and West Nile Virus Mosquito Coinfection and Positive Ecological Association in Chicago, United States
journal, August 2011

  • Newman, Christina M.; Cerutti, Francesco; Anderson, Tavis K.
  • Vector-Borne and Zoonotic Diseases, Vol. 11, Issue 8
  • DOI: 10.1089/vbz.2010.0144

History of domestication and spread of Aedes aegypti - A Review
journal, January 2013

  • Powell, Jeffrey R.; Tabachnick, Walter J.
  • Memórias do Instituto Oswaldo Cruz, Vol. 108, Issue suppl 1
  • DOI: 10.1590/0074-0276130395

Local Mosquito-Borne Transmission of Zika Virus — Miami-Dade and Broward Counties, Florida, June–August 2016
journal, September 2016

  • Likos, Anna; Griffin, Isabel; Bingham, Andrea M.
  • MMWR. Morbidity and Mortality Weekly Report, Vol. 65, Issue 38
  • DOI: 10.15585/mmwr.mm6538e1

Enhanced arbovirus surveillance with deep sequencing: Identification of novel rhabdoviruses and bunyaviruses in Australian mosquitoes
journal, January 2014


Field prevalence of Wolbachia in the mosquito vector Aedes albopictus.
journal, January 2002

  • Baimai, Visut; Kitrayapong, Pattamaporn; O'Neill, Scott L.
  • The American Journal of Tropical Medicine and Hygiene, Vol. 66, Issue 1
  • DOI: 10.4269/ajtmh.2002.66.108

Somatic Wolbachia (Rickettsiales: Rickettsiaceae) Levels in Culex quinquefasciatus and Culex pipiens (Diptera: Culicidae) and Resistance to West Nile Virus Infection
journal, January 2014

  • Micieli, María Victoria; Glaser, Robert L.
  • Journal of Medical Entomology, Vol. 51, Issue 1
  • DOI: 10.1603/me13152

Genomes of viral isolates derived from different mosquitos species
journal, October 2017


Chromobacterium Csp_P Reduces Malaria and Dengue Infection in Vector Mosquitoes and Has Entomopathogenic and In Vitro Anti-pathogen Activities
journal, October 2014


Molecular detection of Wolbachia pipientis in natural populations of mosquito vectors of Dirofilaria immitis from continental Portugal: first detection in Culex theileri
journal, June 2016

  • De Pinho MixÃO, V.; Mendes, A. M.; MaurÍCio, I. L.
  • Medical and Veterinary Entomology, Vol. 30, Issue 3
  • DOI: 10.1111/mve.12179

Comparative analysis of gut microbiota of mosquito communities in central Illinois
journal, February 2017

  • Muturi, Ephantus J.; Ramirez, Jose L.; Rooney, Alejandro P.
  • PLOS Neglected Tropical Diseases, Vol. 11, Issue 2
  • DOI: 10.1371/journal.pntd.0005377

The Elimination of Urban Yellow Fever in the Americas Through the Eradication of Aedes aegypti
journal, January 1963

  • Soper, Fred L.
  • American Journal of Public Health and the Nations Health, Vol. 53, Issue 1
  • DOI: 10.2105/ajph.53.1.7

Prototype endogenous avian retroviruses of the genus Gallus
journal, September 2014

  • Sacco, Melanie Ann; Nair, Venugopal K.
  • Journal of General Virology, Vol. 95, Issue 9
  • DOI: 10.1099/vir.0.066852-0

wMel limits zika and chikungunya virus infection in a Singapore Wolbachia-introgressed Ae. aegypti strain, wMel-Sg
journal, May 2017

  • Tan, Cheong Huat; Wong, PeiSze Jeslyn; Li, Meizhi Irene
  • PLOS Neglected Tropical Diseases, Vol. 11, Issue 5
  • DOI: 10.1371/journal.pntd.0005496

Low genetic diversity in Wolbachia-Infected Culex quinquefasciatus (Diptera: Culicidae) from Brazil and Argentina
journal, December 2012

  • Morais, Sirlei Antunes; Almeida, Fábio de; Suesdek, Lincoln
  • Revista do Instituto de Medicina Tropical de São Paulo, Vol. 54, Issue 6
  • DOI: 10.1590/s0036-46652012000600007

Evaluation of a Field-Portable DNA Microarray Platform and Nucleic Acid Amplification Strategies for the Detection of Arboviruses, Arthropods, and Bloodmeals
journal, February 2013

  • Kengluecha, Ampornpan; Lee, John S.; Pisarcik, Sarah E.
  • The American Journal of Tropical Medicine and Hygiene, Vol. 88, Issue 2
  • DOI: 10.4269/ajtmh.2012.12-0048

Bacterial Communities and Midgut Microbiota Associated with Mosquito Populations from Waste Tires in East-Central Illinois
journal, January 2015

  • Kim, Chang-Hyun; Lampman, Richard L.; Muturi, Ephantus J.
  • Journal of Medical Entomology, Vol. 52, Issue 1
  • DOI: 10.1093/jme/tju011

Experimental Infection with and Maintenance of Cell Fusing Agent Virus (Flavivirus) in Aedes aegypti
journal, July 2017

  • Guzman, Hilda; Thangamani, Saravanan; Contreras-Gutierrez, Maria Angelica
  • The American Journal of Tropical Medicine and Hygiene, Vol. 97, Issue 1
  • DOI: 10.4269/ajtmh.16-0987

A Parvo-like virus persistently infecting a C6/36 clone of Aedes albopictus mosquito cell line and pathogenic for Aedes aegypti larvae
journal, August 1993


Exposure to West Nile Virus Increases Bacterial Diversity and Immune Gene Expression in Culex pipiens
journal, October 2015

  • Zink, Steven; Van Slyke, Greta; Palumbo, Michael
  • Viruses, Vol. 7, Issue 10
  • DOI: 10.3390/v7102886

Cell fusing agent virus and dengue virus mutually interact in Aedes aegypti cell lines
journal, July 2017


Present and future arboviral threats
journal, February 2010


A Wolbachia Symbiont in Aedes aegypti Limits Infection with Dengue, Chikungunya, and Plasmodium
journal, December 2009


Reagent and laboratory contamination can critically impact sequence-based microbiome analyses
journal, November 2014


Genetic Characterization of Zika Virus Strains: Geographic Expansion of the Asian Lineage
journal, February 2012


Analysis of sensitivity and rapid hybridization of a multiplexed Microbial Detection Microarray
journal, June 2014


Wolbachia diversity and cytoplasmic incompatibility patterns in Culex pipiens populations in Turkey
journal, March 2018


Nucleic Acid Sequence-Based Amplification Assays for Rapid Detection of West Nile and St. Louis Encephalitis Viruses
journal, December 2001


Transmission of West Nile Virus by Culex quinquefasciatus Say Infected with Culex Flavivirus Izabal
journal, May 2010


Diversity of Cultivable Midgut Microbiota at Different Stages of the Asian Tiger Mosquito, Aedes albopictus from Tezpur, India
journal, December 2016


Universal diagnostic RT-PCR protocol for arboviruses
journal, May 1998


Application of a pathogen microarray for the analysis of viruses and bacteria in clinical diagnostic samples from pigs
journal, April 2015

  • Jaing, Crystal J.; Thissen, James B.; Gardner, Shea N.
  • Journal of Veterinary Diagnostic Investigation, Vol. 27, Issue 3
  • DOI: 10.1177/1040638715578484

Avian Endogenous Retrovirus EAV-HP Shares Regions of Identity with Avian Leukosis Virus Subgroup J and the Avian Retrotransposon ART-CH
journal, February 2000


Mosquito densonucleosis viruses cause dramatically different infection phenotypes in the C6/36 Aedes albopictus cell line
journal, July 2005


Globalization, Land Use, and the Invasion of West Nile Virus
journal, October 2011


The insect-specific Palm Creek virus modulates West Nile virus infection in and transmission by Australian mosquitoes
journal, July 2016

  • Hall-Mendelin, Sonja; McLean, Breeanna J.; Bielefeldt-Ohmann, Helle
  • Parasites & Vectors, Vol. 9, Issue 1
  • DOI: 10.1186/s13071-016-1683-2

High-Resolution Metatranscriptomics Reveals the Ecological Dynamics of Mosquito-Associated RNA Viruses in Western Australia
journal, June 2017

  • Shi, Mang; Neville, Peter; Nicholson, Jay
  • Journal of Virology, Vol. 91, Issue 17
  • DOI: 10.1128/JVI.00680-17

The Microbial Detection Array for Detection of Emerging Viruses in Clinical Samples - A Useful Panmicrobial Diagnostic Tool
journal, June 2014


The re-emerging arboviral threat: Hidden enemies: The emergence of obscure arboviral diseases, and the potential use of Wolbachia in their control
journal, December 2016

  • Dutra, Heverton Leandro Carneiro; Caragata, Eric Pearce; Moreira, Luciano Andrade
  • BioEssays, Vol. 39, Issue 2
  • DOI: 10.1002/bies.201600175

Nhumirim virus, a novel flavivirus isolated from mosquitoes from the Pantanal, Brazil
journal, September 2014

  • Pauvolid-Corrêa, Alex; Solberg, Owen; Couto-Lima, Dinair
  • Archives of Virology, Vol. 160, Issue 1
  • DOI: 10.1007/s00705-014-2219-8

Distribution and phylogenetic analysis of Culex flavivirus in mosquitoes in China
journal, June 2015


Potential for Co-Infection of a Mosquito-Specific Flavivirus, Nhumirim Virus, to Block West Nile Virus Transmission in Mosquitoes
journal, November 2015

  • Goenaga, Silvina; Kenney, Joan; Duggal, Nisha
  • Viruses, Vol. 7, Issue 11
  • DOI: 10.3390/v7112911

Mosquito vector-associated microbiota: Metabarcoding bacteria and eukaryotic symbionts across habitat types in Thailand endemic for dengue and other arthropod-borne diseases
journal, December 2017

  • Thongsripong, Panpim; Chandler, James Angus; Green, Amy B.
  • Ecology and Evolution, Vol. 8, Issue 2
  • DOI: 10.1002/ece3.3676

Ilheus Virus Isolation in the Pantanal, West-Central Brazil
journal, July 2013

  • Pauvolid-Corrêa, Alex; Kenney, Joan L.; Couto-Lima, Dinair
  • PLoS Neglected Tropical Diseases, Vol. 7, Issue 7
  • DOI: 10.1371/journal.pntd.0002318

The Native Wolbachia Symbionts Limit Transmission of Dengue Virus in Aedes albopictus
journal, December 2012

  • Mousson, Laurence; Zouache, Karima; Arias-Goeta, Camilo
  • PLoS Neglected Tropical Diseases, Vol. 6, Issue 12
  • DOI: 10.1371/journal.pntd.0001989

Assessing the epidemiological effect of wolbachia for dengue control
journal, July 2015


A microbial detection array (MDA) for viral and bacterial detection
journal, January 2010

  • Gardner, Shea N.; Jaing, Crystal J.; McLoughlin, Kevin S.
  • BMC Genomics, Vol. 11, Issue 1
  • DOI: 10.1186/1471-2164-11-668

The entomopathogenic fungus Beauveria bassiana activate toll and JAK-STAT pathway-controlled effector genes and anti-dengue activity in Aedes aegypti
journal, February 2012

  • Dong, Yuemei; Morton, James C.; Ramirez, Jose Luis
  • Insect Biochemistry and Molecular Biology, Vol. 42, Issue 2
  • DOI: 10.1016/j.ibmb.2011.11.005

Ancient pathogen DNA in archaeological samples detected with a Microbial Detection Array
journal, March 2014

  • Devault, Alison M.; McLoughlin, Kevin; Jaing, Crystal
  • Scientific Reports, Vol. 4, Issue 1
  • DOI: 10.1038/srep04245

RNA shotgun metagenomic sequencing of northern California (USA) mosquitoes uncovers viruses, bacteria, and fungi
journal, March 2015

  • Chandler, James Angus; Liu, Rachel M.; Bennett, Shannon N.
  • Frontiers in Microbiology, Vol. 06
  • DOI: 10.3389/fmicb.2015.00185

Studies on Cultured and Uncultured Microbiota of wild Culex Quinquefasciatus Mosquito Midgut Based on 16s Ribosomal rna gene Analysis
journal, June 2004

  • Pidiyar, Vyankatesh J.; Patole, Milind S.; Jangid, Kamlesh
  • The American Journal of Tropical Medicine and Hygiene, Vol. 70, Issue 6
  • DOI: 10.4269/ajtmh.2004.70.597

Genome sequencing and genetic characterization of Culex Flavirirus (CxFV) provides new information about its genotypes
journal, September 2016

  • Bittar, Cíntia; Machado, Daiane Cristina; Vedovello, Danila
  • Virology Journal, Vol. 13, Issue 1
  • DOI: 10.1186/s12985-016-0614-3

Direct broad-range detection of alphaviruses in mosquito extracts
journal, November 2007


Pyrosequencing 16S rRNA genes of bacteria associated with wild tiger mosquito Aedes albopictus: a pilot study
journal, May 2014

  • Minard, Guillaume; Tran, Florence-Hélène; Dubost, Audrey
  • Frontiers in Cellular and Infection Microbiology, Vol. 4
  • DOI: 10.3389/fcimb.2014.00059

Zika in the United States of America and a Fateful 1969 Decision
journal, May 2016


Genetic and Serologic Properties of Zika Virus Associated with an Epidemic, Yap State, Micronesia, 2007
journal, August 2008

  • Lanciotti, Robert S.; Kosoy, Olga L.; Laven, Janeen J.
  • Emerging Infectious Diseases, Vol. 14, Issue 8
  • DOI: 10.3201/eid1408.080287

Culex Flavivirus During West Nile Virus Epidemic and Interepidemic Years in Chicago, United States
journal, August 2017

  • Newman, Christina M.; Krebs, Bethany L.; Anderson, Tavis K.
  • Vector-Borne and Zoonotic Diseases, Vol. 17, Issue 8
  • DOI: 10.1089/vbz.2017.2124

Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from Kenya
journal, September 2012


Multi-Gene Detection and Identification of Mosquito-Borne RNA Viruses Using an Oligonucleotide Microarray
journal, August 2013

  • Grubaugh, Nathan D.; McMenamy, Scott S.; Turell, Michael J.
  • PLoS Neglected Tropical Diseases, Vol. 7, Issue 8
  • DOI: 10.1371/journal.pntd.0002349

Consequences of the Expanding Global Distribution of Aedes albopictus for Dengue Virus Transmission
journal, May 2010


The global compendium of Aedes aegypti and Ae. albopictus occurrence
journal, July 2015

  • Kraemer, Moritz U. G.; Sinka, Marianne E.; Duda, Kirsten A.
  • Scientific Data, Vol. 2, Issue 1
  • DOI: 10.1038/sdata.2015.35

Zika virus in the Americas: Early epidemiological and genetic findings
journal, March 2016

  • Faria, N. R.; Azevedo, R. d. S. d. S.; Kraemer, M. U. G.
  • Science, Vol. 352, Issue 6283
  • DOI: 10.1126/science.aaf5036

Diversity and function of bacterial microbiota in the mosquito holobiont
journal, January 2013

  • Minard, Guillaume; Mavingui, Patrick; Moro, Claire
  • Parasites & Vectors, Vol. 6, Issue 1
  • DOI: 10.1186/1756-3305-6-146

The potential role of Wolbachia in controlling the transmission of emerging human arboviral infections
journal, January 2016

  • Kamtchum-Tatuene, Joseph; Makepeace, Benjamin L.; Benjamin, Laura
  • Current Opinion in Infectious Diseases
  • DOI: 10.1097/QCO.0000000000000342

Detection and clearance of a mosquito densovirus contaminant from laboratory stocks of Zika virus
journal, January 2019

  • Cataneo, Allan Henrique Depieri; Kuczera, Diogo; Mosimann, Ana Luiza Pamplona
  • Memórias do Instituto Oswaldo Cruz, Vol. 114
  • DOI: 10.1590/0074-02760180432

Wolbachia modulates Chikungunya replication in Aedes albopictus
journal, May 2010