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Field application of MALDI-TOF MS on mosquito larvae identification

Published online by Cambridge University Press:  03 August 2017

AMIRA NEBBAK ,
SEKOU KOUMARE ,
ALEXANDRA C. WILLCOX ,
JEAN-MICHEL BERENGER ,
DIDIER RAOULT ,
LIONEL ALMERAS  and
PHILIPPE PAROLA
AMIRA NEBBAK
Affiliation:
Aix Marseille Université, Unité de Recherche en Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198 (Dakar, Sénégal), Inserm 1095, Institut Hospitalo-Universitaire Méditerranée Infection 19-21 Boulevard Jean Moulin 13385 Marseille cedex 05, France Laboratoire de Biodiversité et Environnement: Interactions génomes, Faculté des Sciences Biologiques, Université des Sciences et de la Technologie Houari Boumediene (USTHB), Bab Ezzouar, Algiers, Algeria
SEKOU KOUMARE
Affiliation:
Aix Marseille Université, Unité de Recherche en Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198 (Dakar, Sénégal), Inserm 1095, Institut Hospitalo-Universitaire Méditerranée Infection 19-21 Boulevard Jean Moulin 13385 Marseille cedex 05, France Faculté de médecine, Malaria Research and Training Center, Université de Bamako, BP 1805, Mali
ALEXANDRA C. WILLCOX
Affiliation:
Aix Marseille Université, Unité de Recherche en Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198 (Dakar, Sénégal), Inserm 1095, Institut Hospitalo-Universitaire Méditerranée Infection 19-21 Boulevard Jean Moulin 13385 Marseille cedex 05, France Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
JEAN-MICHEL BERENGER
Affiliation:
Aix Marseille Université, Unité de Recherche en Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198 (Dakar, Sénégal), Inserm 1095, Institut Hospitalo-Universitaire Méditerranée Infection 19-21 Boulevard Jean Moulin 13385 Marseille cedex 05, France
DIDIER RAOULT
Affiliation:
Aix Marseille Université, Unité de Recherche en Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198 (Dakar, Sénégal), Inserm 1095, Institut Hospitalo-Universitaire Méditerranée Infection 19-21 Boulevard Jean Moulin 13385 Marseille cedex 05, France
LIONEL ALMERAS
Affiliation:
Aix Marseille Université, Unité de Recherche en Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198 (Dakar, Sénégal), Inserm 1095, Institut Hospitalo-Universitaire Méditerranée Infection 19-21 Boulevard Jean Moulin 13385 Marseille cedex 05, France Unité de Parasitologie et Entomologie, Département des Maladies Infectieuses, Institut de Recherche Biomédicale des Armées, Marseille, France
PHILIPPE PAROLA*
Affiliation:
Aix Marseille Université, Unité de Recherche en Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198 (Dakar, Sénégal), Inserm 1095, Institut Hospitalo-Universitaire Méditerranée Infection 19-21 Boulevard Jean Moulin 13385 Marseille cedex 05, France
*
*Address for correspondence: Unité de Recherche en Maladies Infectieuses et Tropicales Emergentes (URMITE), Institut Hospitalo-Universitaire Méditerranée Infection, 19-21 bd Jean Moulin, 13385 Marseille cedex 5, France. E-mail: philippe.parola@univ-amu.fr
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Summary

In recent years, matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) has emerged as an efficient tool for arthropod identification. Its application for field monitoring of adult mosquitoes was demonstrated, but identification of larvae has been limited to laboratory-reared specimens. Study aim was to test the success of MALDI-TOF MS in correctly identifying mosquito larvae collected in the field. Collections were performed at 13 breeding sites in urban areas of Marseille, a city in the South of France. A total of 559 larvae were collected. Of these, 73 were accurately morphologically identified, with confirmation either by molecular identification (n = 31) or analysis with MALDI-TOF MS (n = 31) and 11 were tested using both methods. The larvae identified belonged to six species including Culiseta longiareolata, Culex pipiens pipiens, Culex hortensis, Aedes albopictus, Ochlerotatus caspius and Anopheles maculipennis. A high intra-species reproducibility and inter-species specificity of whole larva MS spectra was obtained and was independent of breeding site. More than 92% of the remaining 486 larvae were identified in blind tests against the MS spectra database. Identification rates were lower for early and pupal stages, which is attributed to lower protein abundance and metamorphosis, respectively. The suitability of MALDI-TOF MS for mosquito larvae identification from the field has been confirmed.

Keywords

Mosquito larvae identificationMALDI-TOF MS
Type
Special Issue Article
Information
Parasitology , Volume 145 , Special Issue 5: Advances and challenges in barcoding of microbes, parasites, and their vectors and reservoirs , April 2018 , pp. 677 - 687
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Becker, N., Petrić, D., Zgomba, M., Boase, C., Dahl, C., Madon, M. and Kaiser, A. (2010). Mosquitoes and their Control, 2nd Edn. Springer, Heidelberg, Germany.Google Scholar
Benelli, G. (2016). Spread of Zika virus: the key role of mosquito vector control. Asian Pacific Journal of Tropical Biomedicine 6, 468–471.Google Scholar
Bisanti, M., Ganassi, S. and Mandrioli, M. (2008). Comparative analysis of various fixative solutions on insect preservation for molecular studies. Entomologia Experimentalis et Applicata 130, 290–296.Google Scholar
Bizzini, A., Durussel, C., Bille, J., Greub, G. and Prod'hom, G. (2010). Performance of matrix-assisted laser desorption ionization-time of flight mass spectrometry for identification of bacterial strains routinely isolated in a clinical microbiology laboratory. Journal of Clinical Microbiology 48, 1549–1554.Google Scholar
Cotteaux-Lautard, C., Berenger, J. M., Fusca, F., Chardon, H., Simon, F. and Pages, F. (2013). A new challenge for hospitals in southeast France: monitoring local populations of Aedes albopictus to prevent nosocomial transmission of dengue or chikungunya. Journal of the American Mosquito Control Association 29, 81–83.Google Scholar
Delaunay, P., Jeannin, C., Schaffner, F. and Marty, P. (2009). News on the presence of the tiger mosquito Aedes albopictus in metropolitan France. Archives de Pediatrie 16 (Suppl. 2), S66–S71.Google Scholar
Dieme, C., Yssouf, A., Vega-Rua, A., Berenger, J. M., Failloux, A. B., Raoult, D., Parola, P. and Almeras, L. (2014). Accurate identification of Culicidae at aquatic developmental stages by MALDI-TOF MS profiling. Parasites & Vectors 7, 544.Google Scholar
Dieme, C., Bechah, Y., Socolovschi, C., Audoly, G., Berenger, J. M., Faye, O., Raoult, D. and Parola, P. (2015). Transmission potential of Rickettsia felis infection by Anopheles gambiae mosquitoes. Proceedings of the National Academy of Sciences of the United States of America 112, 8088–8093.Google Scholar
Farajollahi, A., Fonseca, D. M., Kramer, L. D. and Marm, K. A. (2011). ‘Bird biting’ mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. Infection Genetics and Evolution 11, 1577–1585.Google Scholar
Feltens, R., Gorner, R., Kalkhof, S., Groger-Arndt, H. and von Bergen, M. (2010). Discrimination of different species from the genus Drosophila by intact protein profiling using matrix-assisted laser desorption ionization mass spectrometry. BMC Evolutionary Biology 10, 95.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Hoppenheit, A., Murugaiyan, J., Bauer, B., Steuber, S., Clausen, P. H. and Roesler, U. (2013). Identification of Tsetse (Glossina spp.) using matrix-assisted laser desorption/ionisation time of flight mass spectrometry. PLoS Neglected Tropical Diseases 7, e2305.Google Scholar
Impoinvil, D. E., Ahmad, S., Troyo, A., Keating, J., Githeko, A. K., Mbogo, C. M., Kibe, L., Githure, J. I., Gad, A. M., Hassan, A. N., Orshan, L., Warburg, A., Calderon-Arguedas, O., Sanchez-Loria, V. M., Velit-Suarez, R., Chadee, D. D., Novak, R. J. and Beier, J. C. (2007). Comparison of mosquito control programs in seven urban sites in Africa, the Middle East, and the Americas. Health Policy 83, 196–212.Google Scholar
Kaufmann, C., Ziegler, D., Schaffner, F., Carpenter, S., Pfluger, V. and Mathis, A. (2011). Evaluation of matrix-assisted laser desorption/ionization time of flight mass spectrometry for characterization of Culicoides nubeculosus biting midges. Medical And Veterinary Entomology- 25, 32–38.Google Scholar
Kumsa, B., Laroche, M., Almeras, L., Mediannikov, O., Raoult, D. and Parola, P. (2016). Morphological, molecular and MALDI-TOF mass spectrometry identification of ixodid tick species collected in Oromia, Ethiopia. Parasitology Research 115, 4199–4210.Google Scholar
Lafri, I., Almeras, L., Bitam, I., Caputo, A., Yssouf, A., Forestier, C. L., Izri, A., Raoult, D. and Parola, P. (2016). Identification of Algerian field-caught Phlebotomine Sand Fly Vectors by MALDI-TOF MS. PLoS Neglected Tropical Diseases 10, e0004351.Google Scholar
Liu, L. E., Dehning, M., Phipps, A., Swienton, R. E., Harris, C. A. and Klein, K. R. (2016). Clinical update on Dengue, Chikungunya, and Zika: what we know at the time of article submission. Disaster Medicine and Public Health Preparedness, 11, 290–299.Google Scholar
Maria, A. T., Maquart, M., Makinson, A., Flusin, O., Segondy, M., Leparc-Goffart, I., Le Moing, V. and Foulongne, V. (2016). Zika virus infections in three travellers returning from South America and the Caribbean respectively, to Montpellier, France, December 2015 to January 2016. Eurosurveillance 21, 2–5.Google Scholar
McGraw, E. A. and O'Neill, S. L. (2013). Beyond insecticides: new thinking on an ancient problem. Nature Reviews. Microbiology 11, 181–193.Google Scholar
Muller, P., Pfluger, V., Wittwer, M., Ziegler, D., Chandre, F., Simard, F. and Lengeler, C. (2013). Identification of cryptic Anopheles mosquito species by molecular protein profiling. PLoS ONE 8, e57486.Google Scholar
Nebbak, A., Willcox, A. C., Bitam, I., Raoult, D., Parola, P. and Almeras, L. (2016). Standardization of sample homogenization for mosquito identification using an innovative proteomic tool based on protein profiling. Proteomics 16, 3148–3160.Google Scholar
Niare, S., Berenger, J. M., Dieme, C., Doumbo, O., Raoult, D., Parola, P. and Almeras, L. (2016). Identification of blood meal sources in the main African malaria mosquito vector by MALDI-TOF MS. Malaria Journal 15, 87.Google Scholar
Rezza, G. (2014). Dengue and chikungunya: long-distance spread and outbreaks in naive areas. Pathogens and Global Health 108, 349–355.Google Scholar
Rueda, L. M. (2004). Pictorial Keys for the Identification of Mosquitoes (Diptera: Culicidae) Associated with Dengue Virus Transmission. Magnolia Press, Auckland, New Zealand.Google Scholar
Schaffner, F., Angel, G., Geoffroy, B., Hervy, J. P., Rhaiem, A. and Brunhes, J. (2001). The mosquitoes of Europe: an identification and training programme. CD-ROM. IRD Ed., Montpellier. ISBN 2-7099-1485-9.Google Scholar
Schaffner, F., Kaufmann, C., Pfluger, V. and Mathis, A. (2014). Rapid protein profiling facilitates surveillance of invasive mosquito species. Parasites & Vectors 7, 142.Google Scholar
Sim, S., Ramirez, J. L. and Dimopoulos, G. (2009). Molecular discrimination of mosquito vectors and their pathogens. Expert Review of Molecular Diagnostics 9, 757–765.Google Scholar
Steinmann, I. C., Pfluger, V., Schaffner, F., Mathis, A. and Kaufmann, C. (2013). Evaluation of matrix-assisted laser desorption/ionization time of flight mass spectrometry for the identification of ceratopogonid and culicid larvae. Parasitology 140, 318–327.Google Scholar
Suter, T., Flacio, E., Farina, B. F., Engeler, L., Tonolla, M. and Muller, P. (2015). First report of the invasive mosq.uito species Aedes koreicus in the Swiss-Italian border region. Parasites & Vectors 8, 402.Google Scholar
Tolle, M. A. (2009). Mosquito-borne diseases. Current Problems in Pediatric and Adolescent Health Care 39, 97–140.Google Scholar
Wang, G., Li, C., Guo, X., Xing, D., Dong, Y., Wang, Z., Zhang, Y., Liu, M., Zheng, Z., Zhang, H., Zhu, X., Wu, Z. and Zhao, T. (2012). Identifying the main mosquito species in China based on DNA barcoding. PLoS ONE 7, e47051.Google Scholar
Welker, M. and Moore, E. R. (2011). Applications of whole-cell matrix-assisted laser-desorption/ionization time-of-flight mass spectrometry in systematic microbiology. Systematic and Applied Microbiology 34, 2–11.Google Scholar
Yssouf, A., Socolovschi, C., Flaudrops, C., Ndiath, M. O., Sougoufara, S., Dehecq, J. S., Lacour, G., Berenger, J. M., Sokhna, C. S., Raoult, D. and Parola, P. (2013). Matrix-assisted laser desorption ionization--time of flight mass spectrometry: an emerging tool for the rapid identification of mosquito vectors. PLoS ONE 8, e72380.Google Scholar
Yssouf, A., Parola, P., Lindstrom, A., Lilja, T., L'Ambert, G., Bondesson, U., Berenger, J. M., Raoult, D. and Almeras, L. (2014). Identification of European mosquito species by MALDI-TOF MS. Parasitology Research 113, 2375–2378.Google Scholar
Yssouf, A., Almeras, L., Raoult, D. and Parola, P. (2016). Emerging tools for identification of arthropod vectors. Future Microbiology 11, 549–566.Google Scholar
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