Identification of Neotropical Culex Mosquitoes by MALDI-TOF MS Profiling

The mosquito (Diptera: Culicidae) fauna of French Guiana encompasses 242 species, of which nearly half of them belong to the genus Culex. Whereas several species of Culex are important vectors of arboviruses, only a limited number of studies focus on them due to the difficulties to morphologically identify field-caught females. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) has been reported as a promising method for the identification of mosquitoes. Culex females collected in French Guiana were morphologically identified and dissected. Abdomens were used for molecular identification using the COI (cytochrome oxidase 1) gene. Legs and thorax of 169 specimens belonging to 13 Culex species, (i.e., Cx. declarator, Cx. nigripalpus, Cx. quinquefasciatus, Cx. usquatus, Cx. adamesi, Cx. dunni, Cx. eastor, Cx. idottus, Cx. pedroi, Cx. phlogistus, Cx. portesi, Cx. rabanicolus and Cx. spissipes) were then submitted to MALDI-TOF MS analysis. A high intra-species reproducibility and inter-species specificity of MS spectra for each mosquito body part tested were obtained. A corroboration of the specimen identification was revealed between MALDI-TOF MS, morphological and molecular results. MALDI-TOF MS protein profiling proves to be a suitable tool for identification of neotropical Culex species and will permit the enhancement of knowledge on this highly diverse genus.

[1]  P. Parola,et al.  Enhanced procedures for mosquito identification by MALDI-TOF MS , 2022, Parasites & vectors.

[2]  P. Parola,et al.  MALDI-TOF mass spectrometry identification of mosquitoes collected in Vietnam , 2022, Parasites & vectors.

[3]  S. D. Del Valle,et al.  Updated distribution maps of predominant Culex mosquitoes across the Americas , 2021, Parasites & vectors.

[4]  O. Doumbo,et al.  High-throughput detection of eukaryotic parasites and arboviruses in mosquitoes , 2021, Biology open.

[5]  J. Drexler,et al.  Venezuelan Equine Encephalitis Complex Alphavirus in Bats, French Guiana , 2021, Emerging infectious diseases.

[6]  P. Parola,et al.  Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry: an emerging tool for studying the vectors of human infectious diseases. , 2021, Future microbiology.

[7]  O. Doumbo,et al.  New assessment of Anopheles vector species identification using MALDI-TOF MS , 2021, Malaria journal.

[8]  J. Duchemin,et al.  The Culex Mosquitoes (Diptera: Culicidae) of French Guiana: A Comprehensive Review With the Description of Three New Species , 2020, Journal of Medical Entomology.

[9]  A. Tarantola,et al.  MALDI-TOF MS: optimization for future uses in entomological surveillance and identification of mosquitoes from New Caledonia , 2020, Parasites & Vectors.

[10]  P. Somboon,et al.  A Multiplex PCR Based on Mitochondrial COI Sequences for Identification of Members of the Anopheles barbirostris Complex (Diptera: Culicidae) in Thailand and Other Countries in the Region , 2020, Insects.

[11]  S. Briolant,et al.  Identification of French Guiana anopheline mosquitoes by MALDI-TOF MS profiling using protein signatures from two body parts , 2020, bioRxiv.

[12]  R. Lowen,et al.  Complete genomic sequences of Venezuelan equine encephalitis virus subtype IIID isolates from mosquitoes , 2020, Archives of Virology.

[13]  Durrell D. Kapan,et al.  Patterns, Drivers, and Challenges of Vector-Borne Disease Emergence. , 2019, Vector borne and zoonotic diseases.

[14]  Mathieu Nacher,et al.  Discriminating Tonate Virus from Dengue Virus Infection: A Matched Case–Control Study in French Guiana, 2003–2016 , 2019, The American journal of tropical medicine and hygiene.

[15]  A. Mondini,et al.  Ecological aspects of potential arbovirus vectors (Diptera: Culicidae) in an urban landscape of Southern Amazon, Brazil. , 2019, Acta tropica.

[16]  T. Andreadis,et al.  West Nile Virus Mosquito Vectors in North America , 2019, Journal of Medical Entomology.

[17]  N. Johnson,et al.  DNA barcoding of British mosquitoes (Diptera, Culicidae) to support species identification, discovery of cryptic genetic diversity and monitoring invasive species , 2019, ZooKeys.

[18]  R. Piarroux,et al.  Identification of French Guiana sand flies using MALDI-TOF mass spectrometry with a new mass spectra library , 2019, PLoS neglected tropical diseases.

[19]  S. Briolant,et al.  Longitudinal monitoring of environmental factors at Culicidae larval habitats in urban areas and their association with various mosquito species using an innovative strategy. , 2018, Pest management science.

[20]  J. Gustave,et al.  Improvement of mosquito identification by MALDI-TOF MS biotyping using protein signatures from two body parts , 2018, Parasites & Vectors.

[21]  S. Sawalha,et al.  Identification of mosquitoes (Diptera: Culicidae): an external quality assessment of medical entomology laboratories in the MediLabSecure Network , 2018, Parasites & Vectors.

[22]  J. Šlapeta,et al.  Accurate identification of Australian mosquitoes using protein profiling , 2018, Parasitology.

[23]  N. Burkett-Cadena,et al.  Vertebrate Hosts of Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus (Diptera: Culicidae) as Potential Vectors of Zika Virus in Florida , 2018, Journal of Medical Entomology.

[24]  F. Tandina,et al.  Blood meal identification in the cryptic species Anopheles gambiae and Anopheles coluzzii using MALDI-TOF MS , 2018, Parasite.

[25]  K. Emerson,et al.  Molecular phylogeny of Culex subgenus Melanoconion (Diptera: Culicidae) based on nuclear and mitochondrial protein-coding genes , 2018, Royal Society Open Science.

[26]  D. Raoult,et al.  Assessment of MALDI-TOF mass spectrometry for filariae detection in Aedes aegypti mosquitoes , 2017, PLoS neglected tropical diseases.

[27]  L. F. Chaves,et al.  Enzootic mosquito vector species at equine encephalitis transmission foci in the República de Panamá , 2017, PloS one.

[28]  S. Boyer,et al.  Usefulness and accuracy of MALDI‐TOF mass spectrometry as a supplementary tool to identify mosquito vector species and to invest in development of international database , 2017, Medical and veterinary entomology.

[29]  D. Raoult,et al.  Field application of MALDI-TOF MS on mosquito larvae identification , 2017, Parasitology.

[30]  O. Doumbo,et al.  Molecular and MALDI-TOF identification of ticks and tick-associated bacteria in Mali , 2017, PLoS neglected tropical diseases.

[31]  D. Raoult,et al.  Standardization of sample homogenization for mosquito identification using an innovative proteomic tool based on protein profiling , 2016, Proteomics.

[32]  A. Karger.  Current developments to use linear MALDI‐TOF spectra for the identification and typing of bacteria and the characterization of other cells/organisms related to infectious diseases , 2016, Proteomics. Clinical applications.

[33]  Romain Girod,et al.  Detection of Chikungunya Virus Circulation Using Sugar-Baited Traps during a Major Outbreak in French Guiana , 2016, PLoS neglected tropical diseases.

[34]  S. Briolant,et al.  High malaria transmission in a forested malaria focus in French Guiana: How can exophagic Anopheles darlingi thwart vector control and prevention measures? , 2016, Memorias do Instituto Oswaldo Cruz.

[35]  D. Raoult,et al.  Emerging tools for identification of arthropod vectors. , 2016, Future microbiology.

[36]  N. Bergman,et al.  Identification and Genomic Analysis of a Novel Group C Orthobunyavirus Isolated from a Mosquito Captured near Iquitos, Peru , 2016, PLoS neglected tropical diseases.

[37]  Romain Girod,et al.  Differential Susceptibilities of Aedes aegypti and Aedes albopictus from the Americas to Zika Virus , 2016, PLoS neglected tropical diseases.

[38]  O. Doumbo,et al.  Identification of blood meal sources in the main African malaria mosquito vector by MALDI-TOF MS , 2016, Malaria Journal.

[39]  S. Briolant,et al.  Malaria in French Guiana Linked to Illegal Gold Mining , 2016, Emerging infectious diseases.

[40]  F. Pagés,et al.  Epidemiological and entomological studies of a malaria outbreak among French armed forces deployed at illegal gold mining sites reveal new aspects of the disease’s transmission in French Guiana , 2016, Malaria Journal.

[41]  D. Raoult,et al.  Identification of Algerian Field-Caught Phlebotomine Sand Fly Vectors by MALDI-TOF MS , 2016, PLoS neglected tropical diseases.

[42]  A. Dejean,et al.  Updated Checklist of the Mosquitoes (Diptera: Culicidae) of French Guiana , 2015, Journal of medical entomology.

[43]  A. Vujić,et al.  DNA barcoding applied: identifying the larva of Merodon avidus (Diptera: Syrphidae) , 2014 .

[44]  D. Raoult,et al.  Accurate identification of Culicidae at aquatic developmental stages by MALDI-TOF MS profiling , 2014, Parasites & Vectors.

[45]  B. Alto,et al.  Reproductive biology and susceptibility of Florida Culex coronator to infection with West Nile virus. , 2014, Vector borne and zoonotic diseases.

[46]  W. Almirón,et al.  COI barcode versus morphological identification of Culex ( Culex ) (Diptera: Culicidae) species: a case study using samples from Argentina and Brazil , 2013, Memorias do Instituto Oswaldo Cruz.

[47]  A. Githeko,et al.  A first report of Anopheles funestus sibling species in western Kenya highlands. , 2013, Acta tropica.

[48]  D. Raoult,et al.  Matrix-Assisted Laser Desorption Ionization - Time of Flight Mass Spectrometry: An Emerging Tool for the Rapid Identification of Mosquito Vectors , 2013, PloS one.

[49]  C. Lengeler,et al.  Identification of Cryptic Anopheles Mosquito Species by Molecular Protein Profiling , 2013, PloS one.

[50]  M. Sallum,et al.  A multi-locus approach to barcoding in the Anopheles strodei subgroup (Diptera: Culicidae) , 2013, Parasites & Vectors.

[51]  J. Ehrenberg,et al.  Lymphatic filariasis in Brazil: epidemiological situation and outlook for elimination , 2012, Parasites & Vectors.

[52]  Romain Girod,et al.  Incrimination of Anopheles (Anopheles) intermedius Peryassú, An. (Nyssorhynchus) nuneztovari Gabaldón, An. (Nys.) oswaldoi Peryassú as natural vectors of Plasmodium falciparum in French Guiana. , 2012, Memorias do Instituto Oswaldo Cruz.

[53]  R. Harbach.  Classification within the cosmopolitan genus Culex (Diptera: Culicidae): the foundation for molecular systematics and phylogenetic research. , 2011, Acta tropica.

[54]  Motomi Ito,et al.  Current progress in DNA barcoding and future implications for entomology , 2011 .

[55]  R. Lourenço-de-Oliveira,et al.  Caiman-Biting Mosquitoes and the Natural Vectors of Hepatozoon caimani in Brazil , 2010, Journal of medical entomology.

[56]  M. Williamson,et al.  Development of multiplex real-time PCR assays for identification of members of the Anopheles funestus species group , 2009, Malaria Journal.

[57]  A. P. Adams,et al.  Isolation and phylogenetic analysis of Mucambo virus (Venezuelan equine encephalitis complex subtype IIIA) in Trinidad. , 2009, Virology.

[58]  D. Raoult,et al.  Ongoing revolution in bacteriology: routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. , 2009, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[59]  R. Kent.  Molecular methods for arthropod bloodmeal identification and applications to ecological and vector‐borne disease studies , 2009, Molecular ecology resources.

[60]  R. Wilkerson,et al.  Insight into Global Mosquito Biogeography from Country Species Records , 2007, Journal of medical entomology.

[61]  P. Hebert,et al.  bold: The Barcode of Life Data System (http://www.barcodinglife.org) , 2007, Molecular ecology notes.

[62]  E. Cupp,et al.  West Nile Virus Infection in Mosquitoes in the Mid-South USA, 2002–2005 , 2007, Journal of medical entomology.

[63]  J. Guerrero,et al.  Epidemiology of heartworm: what is happening in South America and Mexico? , 2005, Veterinary parasitology.

[64]  H. Guzmán,et al.  Isolation of Viruses from Mosquitoes (Diptera: Culicidae) Collected in the Amazon Basin Region of Peru , 2005, Journal of medical entomology.

[65]  S. Weaver,et al.  Natural Enzootic Vectors of Venezuelan equine encephalitis virus in the Magdalena Valley, Colombia , 2003, Emerging infectious diseases.

[66]  M. Turell,et al.  Vector competence of selected North American Culex and Coquillettidia mosquitoes for West Nile virus. , 2001, Emerging infectious diseases.

[67]  A. Failloux,et al.  Aedes aegypti in French Guiana: susceptibility to a dengue virus , 2001, Tropical medicine & international health : TM & IH.

[68]  M. Sallum,et al.  Revision of the Spissipes Section of Culex (Melanoconion) (Diptera:Culicidae). , 1996, Journal of the American Mosquito Control Association.

[69]  O. P. Forattini,et al.  Principais mosquitos de importância sanitária no Brasil , 1995 .

[70]  R. Vrijenhoek,et al.  DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. , 1994, Molecular marine biology and biotechnology.

[71]  F. Collins,et al.  The internal transcribed spacers of ribosomal DNA in five members of the Anopheles gambiae species complex , 1994, Insect molecular biology.

[72]  G. A. Curtis,et al.  Annual emergence patterns of Culex nigripalpus females before, during and after a widespread St. Louis encephalitis epidemic in south Florida. , 1993, Journal of the American Mosquito Control Association.

[73]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[74]  R. A. Ward,et al.  INDEX TO THE SECOND SUPPLEMENT TO “A CATALOG OF THE MOSQUITOES OF THE WORLD” WITH CORRECTIONS AND ADDITIONS , 1985 .

[75]  R. A. Ward,et al.  Index to the Second Supplement to "A Catalog of the Mosquitoes of the Yorld", with Corrections and Additions (Diptera: Culicidae) , 1985 .

[76]  Nicolas Dégallier.  Les arbovirus selvatiques en Guyane française et leurs vecteurs , 1982 .

[77]  S. Sirivanakarn.  A Review of the Systematics and a Proposed Scheme of Internal Classification of the New World Subgenus Melanoconion of Culex (Diptera, Culicidae) , 1982 .

[78]  K. Knight,et al.  A catalog of the mosquitoes of the world (Diptera : Culicidae) , 1977 .

[79]  P. Lajudie,et al.  Streptococci, Dick reaction and endemic lymphangitis in French Guiana. , 1945 .