Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T03:10:53.180Z Has data issue: false hasContentIssue false
  • English
  • Français

Accurate identification of Australian mosquitoes using protein profiling

Published online by Cambridge University Press:  01 October 2018

Andrea L. Lawrence ,
Jana Batovska ,
Cameron E. Webb ,
Stacey E. Lynch ,
Mark J. Blacket ,
Jan Šlapeta Open the ORCID record for Jan Šlapeta [Opens in a new window] ,
Philippe Parola  and
Maureen Laroche Open the ORCID record for Maureen Laroche [Opens in a new window]
Andrea L. Lawrence
Affiliation:
Marie Bashir Institute of Infectious Diseases and Biosecurity, University of Sydney, Sydney, New South Wales 2006, Australia Medical Entomology, NSW Health Pathology, ICPMR, Westmead Hospital, Westmead, New South Wales 2145, Australia Sydney School of Veterinary Science, Faculty of Science, University of Sydney, Sydney, New South Wales 2006, Australia
Jana Batovska
Affiliation:
Agriculture Victoria, AgriBio, Centre for AgriBioscience, Bundoora, Victoria 3083, Australia School of Applied Systems Biology, La Trobe University, Bundoora, Victoria 3083, Australia
Cameron E. Webb
Affiliation:
Marie Bashir Institute of Infectious Diseases and Biosecurity, University of Sydney, Sydney, New South Wales 2006, Australia Medical Entomology, NSW Health Pathology, ICPMR, Westmead Hospital, Westmead, New South Wales 2145, Australia
Stacey E. Lynch
Affiliation:
Agriculture Victoria, AgriBio, Centre for AgriBioscience, Bundoora, Victoria 3083, Australia
Mark J. Blacket
Affiliation:
Agriculture Victoria, AgriBio, Centre for AgriBioscience, Bundoora, Victoria 3083, Australia
Jan Šlapeta
Affiliation:
Sydney School of Veterinary Science, Faculty of Science, University of Sydney, Sydney, New South Wales 2006, Australia
Philippe Parola
Affiliation:
Aix Marseille University, IRD, AP-HM, SSA, VITROME, IHU-Méditerranée Infection, 19-21 Boulevard Jean Moulin 13005 Marseille, France
Maureen Laroche*
Affiliation:
Aix Marseille University, IRD, AP-HM, SSA, VITROME, IHU-Méditerranée Infection, 19-21 Boulevard Jean Moulin 13005 Marseille, France
*
Author for correspondence: Maureen Laroche, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Australian mosquito species significantly impact human health through nuisance biting and the transmission of endemic and exotic pathogens. Surveillance programmes designed to provide an early warning of mosquito-borne disease risk require reliable identification of mosquitoes. This study aimed to investigate the viability of Matrix-Assisted Laser Desorption/Ionization–Time-of-Flight Mass Spectrometry (MALDI-TOF MS) as a rapid and inexpensive approach to the identification of Australian mosquitoes and was validated using a three-step taxonomic approach. A total of 300 mosquitoes representing 21 species were collected from south-eastern New South Wales and morphologically identified. The legs from the mosquitoes were removed and subjected to MALDI-TOF MS analysis. Fifty-eight mosquitoes were sequenced at the cytochrome c oxidase subunit I (cox1) gene region and genetic relationships were analysed. We create the first MALDI-TOF MS spectra database of Australian mosquito species including 19 species. We clearly demonstrate the accuracy of MALDI-TOF MS for identification of Australian mosquitoes. It is especially useful for assessing gaps in the effectiveness of DNA barcoding by differentiating closely related taxa. Indeed, cox1 DNA barcoding was not able to differentiate members of the Culex pipiens group, Cx. quinquefasciatus and Cx. pipiens molestus, but these specimens were correctly identified using MALDI-TOF MS.

Keywords

DNA barcodingidentificationMALDI-TOF MSmosquitoesprotein profilingsurveillance
Type
Research Article
Information
Parasitology , Volume 146 , Issue 4 , April 2019 , pp. 462 - 471
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Batovska, J, Blacket, MJ, Brown, K and Lynch, SE (2016) Molecular identification of mosquitoes (Diptera: Culicidae) in southeastern Australia. Ecology and Evolution 6, 3001–3011.Google Scholar
Batovska, J, Lynch, SE, Cogan, NOI, Brown, K, Darbro, JM, Kho, EA and Blacket, MJ (2017) Effective mosquito and arbovirus surveillance using metabarcoding. Molecular Ecology Resources 18, 32–40.Google Scholar
Boucheikhchoukh, M, Laroche, M, Aouadi, A, Dib, L, Benakhla, A, Raoult, D and Parola, P (2018) MALDI-TOF MS identification of ticks of domestic and wild animals in Algeria and molecular detection of associated microorganisms. Comparative Immunology, Microbiology and Infectious Diseases 57, 39–49.Google Scholar
Burrow, JNC, Whelan, PI, Kilburn, CJ, Fisher, DA, Currie, BJ and Smith, DW (1998) Australian encephalitis in the Northern Territory: clinical and epidemiological features, 1987–1996. Australian and New Zealand Journal of Medicine 28, 590–596.Google Scholar
Claflin, SB and Webb, CE (2015) Ross River virus: many vectors and unusual hosts make for an unpredictable pathogen. PLoS Pathogens 11, e1005070.Google Scholar
Dieme, C, Yssouf, A, Vega-Rúa, 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
Dobrotworsky, NV (1965) The Mosquitoes of Victoria (Diptera, Culicidae). Carlton, Victoria, Australia: Melbourne University Press.Google Scholar
Dridi, B, Raoult, D and Drancourt, M (2012) Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry identification of Archaea: towards the universal identification of living organisms. APMIS 120, 85–91.Google Scholar
Dvorak, V, Halada, P, Hlavackova, K, Dokianakis, E, Antoniou, M and Volf, P (2014) Identification of phlebotomine sand flies (Diptera: Psychodidae) by matrix-assisted laser desorption/ionization time of flight mass spectrometry. Parasites & Vectors 7, 21.Google Scholar
Endersby, NM, White, VL, Chan, J, Hurst, T, Rašić, G, Miller, A and Hoffmann, AA (2013) Evidence of cryptic genetic lineages within Aedes notoscriptus (Skuse). Infection, Genetics and Evolution 18, 191–201.Google Scholar
Flaudrops, C, Faye, N, Mediannikov, O, Sokhna, C, Lo, CI, Fall, B, Sambe-Ba, B, Wade, B, Raoult, D, Fenollar, F (2017) Value of matrix assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometry in clinical microbiology and infectious diseases in Africa and tropical areas. African Journal of Microbiology Research 11, 1360–1370.Google Scholar
Flies, EJ, Toi, C, Weinstein, P, Doggett, SL and Williams, CR (2015) Converting mosquito surveillance to arbovirus surveillance with honey-baited nucleic acid preservation cards. Vector-Borne and Zoonotic Diseases 15, 397–403.Google Scholar
Foley, DH, Wilkerson, RC, Cooper, RD, Volovsek, ME and Bryan, JH (2007) A molecular phylogeny of Anopheles annulipes (Diptera: Culicidae) sensu lato: the most species-rich anopheline complex. Molecular Phylogenetics and Evolution 43, 283–297.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
Fonseca, DM, Keyghobadi, N, Malcolm, CA, Mehmet, C, Schaffner, F, Mogi, M, Fleischer, RC and Wilkerson, RC (2004) Emerging vectors in the Culex pipiens complex. Science 303, 1535–1538.Google Scholar
Hall-Mendelin, S, Pyke, AT, Moore, PR, Mackay, IM, McMahon, JL, Ritchie, SA, Taylor, CT, Moore, FAJ and van den Hurk, AF (2016) Assessment of local mosquito species incriminates Aedes aegypti as the potential vector of Zika virus in Australia. PLoS Neglected Tropical Diseases 10, e0004959.Google Scholar
Harley, D, Sleigh, A and Ritchie, S (2001) Ross River virus transmission, infection, and disease: a cross-disciplinary review. Clinical Microbiology Reviews 14, 909–932.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
Jacups, SP, Whelan, PI and Currie, BJ (2008) Ross River virus and Barmah Forest virus infections: a review of history, ecology, and predictive models, with implications for tropical northern Australia. Vector-Borne and Zoonotic Diseases 8, 283–298.Google Scholar
Jansen, CC and Beebe, NW (2010) The dengue vector Aedes aegypti: what comes next. Microbes and Infection 12, 272–279.Google Scholar
Karger, A, Kampen, H, Bettin, B, Dautel, H, Ziller, M, Hoffmann, B, Süss, J and Klaus, C (2012) Species determination and characterization of developmental stages of ticks by whole-animal matrix-assisted laser desorption/ionization mass spectrometry. Ticks and Tick-Borne Diseases 3, 78–89.Google Scholar
Kassim, NFA, Webb, CE and Russell, RC (2012) Culex molestus Forskal (Diptera: Culicidae) in Australia: colonisation, stenogamy, autogeny, oviposition and larval development. Austral Entomology 51, 67–77.Google Scholar
Kaufmann, C, Schaffner, F, Ziegler, D, Pflueger, V and Mathis, A (2012) Identification of field-caught Culicoides biting midges using matrix-assisted laser desorption/ionization time of flight mass spectrometry. Parasitology 139, 248–258.Google Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P and Drummond, A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.Google Scholar
La Scola, B, Campocasso, A, N'Dong, R, Fournous, G, Barrassi, L, Flaudrops, C and Raoult, D (2010) Tentative characterization of new environmental giant viruses by MALDI-TOF mass spectrometry. Intervirology 53, 344–353.Google Scholar
Laroche, M, Almeras, L, Pecchi, E, Bechah, Y, Raoult, D, Viola, A and Parola, P (2017 a) MALDI-TOF MS as an innovative tool for detection of Plasmodium parasites in Anopheles mosquitoes. Malaria Journal 16, 5.Google Scholar
Laroche, M, Bérenger, J-M, Gazelle, G, Blanchet, D, Raoult, D and Parola, P (2017 b) MALDI-TOF MS protein profiling for the rapid identification of Chagas disease triatomine vectors and application to the triatomine fauna of French Guiana. Parasitology 145, 665–675.Google Scholar
Lee, DJ, Hicks, MM, Debenham, ML, Griffiths, M, Marks, EN, Bryan, JH and Russell, RC (1989) The Culicidae of the Australian Region: Volume 7. Canberra, Australia: ACT, Australian Government Printing Service.Google Scholar
Lilja, T, Nylander, JAA, Troell, K and Lindström, A (2017) Species identification of Swedish mosquitoes through DNA metabarcoding. Control Association 35, 1–9.Google Scholar
Lin, Z and Cai, Z (2018) Negative ion laser desorption/ionization time-of-flight mass spectrometric analysis of small molecules by using nanostructured substrate as matrices. Mass Spectrometry Reviews 37, 681–696.Google Scholar
Mackenzie, JS, Lindsay, MD, Coelen, RJ, Broom, AK, Hall, RA and Smith, DW (1994) Arboviruses causing human disease in the Australasian zoogeographic region. Archives of Virology 136, 447–467.Google Scholar
Mackenzie, JS, Johansen, CA, Ritchie, SA, Van Den Hurk, AF, Hall, RA (2002) Japanese encephalitis as an emerging virus: the emergence and spread of Japanese encephalitis virus in Australasia. In Mackenzie, JS, Barrett, ADT and Deubel, V (eds) Japanese Encephalitis and West Nile Viruses. Springer, Berlin, Heidelberg, pp. 49–73.Google Scholar
Mathis, A, Depaquit, J, Dvořák, V, Tuten, H, Bañuls, A-L, Halada, P, Zapata, S, Lehrter, V, Hlavačková, K, Prudhomme, J, Volf, P, Sereno, D, Kaufmann, C, Pflüger, V and Schaffner, F (2015) Identification of phlebotomine sand flies using one MALDI-TOF MS reference database and two mass spectrometer systems. Parasites & Vectors 8, 266.Google Scholar
Mewara, A, Sharma, M, Kaura, T, Zaman, K, Yadav, R and Sehgal, R (2018) Rapid identification of medically important mosquitoes by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Parasites & Vectors 11, 281.Google Scholar
Montgomery, BL, Shivas, MA, Hall-Mendelin, S, Edwards, J, Hamilton, NA, Jansen, CC, McMahon, JL, Warrilow, D and van den Hurk, AF (2017) Rapid Surveillance for Vector Presence (RSVP): development of a novel system for detecting Aedes aegypti and Aedes albopictus. PLoS Neglected Tropical Diseases 11, e0005505.Google Scholar
Müller, P, Pflüger, 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, AC, 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
Nett, RJ, Campbell, GL and Reisen, WK (2008) Potential for the emergence of Japanese encephalitis virus in California. Vector-Borne and Zoonotic Diseases 9, 511–517.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, 1–15.Google Scholar
Raharimalala, FN, Andrianinarivomanana, TM, Rakotondrasoa, A, Collard, JM and Boyer, S (2017) 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. Medical and Veterinary Entomology 31, 289–298.Google Scholar
Ritchie, SA, Van Den Hurk, AF, Zborowski, P, Kerlin, TJ, Banks, D, Walker, JA, Lee, JM, Montgomery, BL, Smith, GA and Pyke, AT (2007) Operational trials of remote mosquito trap systems for Japanese encephalitis virus surveillance in the Torres Strait, Australia. Vector-Borne and Zoonotic Diseases 7, 497–506.Google Scholar
Russell, RC (1993) Mosquitoes and Mosquito-Borne Disease in Southeastern Australia. Sydney: University of Sydney Printing Service, NSW.Google Scholar
Russell, RC (1995) Arboviruses and their vectors in Australia: an update on the ecology and epidemiology of some mosquito-borne arboviruses. Review of Medical and Veterinary Entomology (United Kingdom). Department of Medical Entomology, Westmead Hospital and the University of Sydney.Google Scholar
Russell, RC (1996) A colour photo atlas of mosquitoes of southeastern Australia, R.C. Russell, Sydney, Australia.Google Scholar
Ryan, PA and Kay, BH (1999) Vector competence of mosquitoes (Diptera: Culicidae) from Maroochy Shire, Australia, for Barmah Forest virus. Journal of Medical Entomology 36, 856–860.Google Scholar
Schaffner, F, Kaufmann, C, Pflüger, V and Mathis, A (2014) Rapid protein profiling facilitates surveillance of invasive mosquito species. Parasites & Vectors 7, 1–7.Google Scholar
Selvey, LA, Dailey, L, Lindsay, M, Armstrong, P, Tobin, S, Koehler, AP, Markey, PG and Smith, DW (2014) The changing epidemiology of Murray Valley encephalitis in Australia: the 2011 outbreak and a review of the literature. PLoS Neglected Tropical Diseases 8, e2656.Google Scholar
Seng, P, Rolain, J-M, Fournier, PE, La Scola, B, Drancourt, M and Raoult, D (2010) MALDI-TOF-mass spectrometry applications in clinical microbiology. Future Microbiology 5, 1733–1754.Google Scholar
Shaikevich, EV, Vinogradova, EB, Bouattour, A and Gouveia de Almeida, AP (2016) Genetic diversity of Culex pipiens mosquitoes in distinct populations from Europe: contribution of Cx. quinquefasciatus in Mediterranean populations. Parasites & Vectors 9, 47.Google Scholar
Smith, JL and Fonseca, DM (2004) Rapid assays for identification of members of the Culex (culex) pipiens complex, their hybrids, and other sibling species (Diptera: Culicidae). The American Journal of Tropical Medicine and Hygiene 70, 339–345.Google Scholar
Tompkins, DM and Gleeson, DM (2006) Relationship between avian malaria distribution and an exotic invasive mosquito in New Zealand. Journal of the Royal Society of New Zealand 36, 51–62.Google Scholar
Tran, T-N-N, Aboudharam, G, Gardeisen, A, Davoust, B, Bocquet-Appel, J-P, Flaudrops, C, Belghazi, M, Raoult, D and Drancourt, M (2011) Classification of ancient mammal individuals using dental pulp MALDI-TOF MS peptide profiling. PLoS ONE 6, e17319.Google Scholar
van den Hurk, AF, Hall-Mendelin, S, Johansen, CA, Warrilow, D and Ritchie, SA (2012) Evolution of mosquito-based arbovirus surveillance systems in Australia. BioMed Research International 2012, Article ID 325659, 1–8.Google Scholar
van den Hurk, AF, Hall-Mendelin, S, Townsend, M, Kurucz, N, Edwards, J, Ehlers, G, Rodwell, C, Moore, FA, McMahon, JL and Northill, JA (2014) Applications of a sugar-based surveillance system to track arboviruses in wild mosquito populations. Vector-Borne and Zoonotic Diseases 14, 66–73.Google Scholar
van den Hurk, AF, Nicholson, J, Beebe, NW, Davis, J, Muzari, OM, Russell, RC, Devine, GJ and Ritchie, SA (2016) Ten years of the Tiger: Aedes albopictus presence in Australia since its discovery in the Torres Strait in 2005. One Health 2, 19–24.Google Scholar
Webb, CE and Doggett, SL (2016) Exotic mosquito threats require strategic surveillance and response planning. Public Health Research & Practice 26.Google Scholar
Webb, C, Russell, R and Doggett, S (2016) A Guide to Mosquitoes of Australia. CSIRO Publishing, Australia.Google Scholar
Whiteman Noah, K, Goodman Simon, J, Sinclair Bradley, J, Walsh, TIM, Cunningham Andrew, A, Kramer Laura, D and Parker Patricia, G (2005) Establishment of the avian disease vector Culex quinquefasciatus Say, 1823 (Diptera: Culicidae) on the Galápagos Islands, Ecuador. Ibis 147, 844–847Google Scholar
Williams, CR, Ritchie, SA and Whelan, PI (2005) Potential distribution of the Asian disease vector Culex gelidus Theobald (Diptera: Culicidae) in Australia and New Zealand: a prediction based on climate suitability. Austral Entomology 44, 425–430.Google Scholar
Williams Craig, R, Bader Christie, A, Williams Samantha, R and Whelan Peter, I (2012) Adult mosquito trap sensitivity for detecting exotic mosquito incursions and eradication: a study using EVS traps and the Australian southern saltmarsh mosquito, Aedes camptorhynchus. Journal of Vector Ecology 37, 110–116.Google Scholar
Yssouf, A, Flaudrops, C, Drali, R, Kernif, T, Socolovschi, C, Berenger, J-M, Raoult, D and Parola, P (2013 a) Matrix-Assisted Laser Desorption Ionization–Time of Flight Mass Spectrometry for rapid identification of tick vectors. Journal of Clinical Microbiology 51, 522–528.Google Scholar
Yssouf, A, Socolovschi, C, Flaudrops, C, Ndiath, MO, Sougoufara, S, Dehecq, J-S, Lacour, G, Berenger, J-M, Sokhna, CS, Raoult, D and Parola, P (2013 b) 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, Lindström, A, Lilja, T, L'Ambert, G, Bondesson, U, Berenger, J-M, Raoult, D and Almeras, L (2014 a) Identification of European mosquito species by MALDI-TOF MS. Parasitology Research 113, 2375–2378.Google Scholar
Yssouf, A, Socolovschi, C, Leulmi, H, Kernif, T, Bitam, I, Audoly, G, Almeras, L, Raoult, D and Parola, P (2014 b) Identification of flea species using MALDI-TOF/MS. Comparative Immunology, Microbiology and Infectious Diseases 37, 153–157.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
Supplementary material: File

Lawrence et al. supplementary material

Table S1

Download Lawrence et al. supplementary material(File)
File 142.5 KB
Supplementary material: File

Lawrence et al. supplementary material

Lawrence et al. supplementary material 1

Download Lawrence et al. supplementary material(File)
File 39.1 KB
Supplementary material: File

Lawrence et al. supplementary material

Lawrence et al. supplementary material 2

Download Lawrence et al. supplementary material(File)
File 17.1 MB