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Issue: Vol. 5339 No. 2: 29 Aug. 2023
Type: Article
Published: 2023-08-29
DOI: 10.11646/zootaxa.5339.2.3
Page range: 159-176
Abstract views: 416
PDF downloaded: 100

Catalase enzymatic activity in adult mosquitoes (Diptera: Culicidae): taxonomic distribution of the continuous trait suggests its relevance for phylogeny research

Zoological Institute; Russian Academy of Sciences; Universitetskaya nab.; 1; St Petersburg; 199034; Russia
Diptera antioxidant enzyme hydrogen peroxide decomposition affinity of genera Coquillettidia Culiseta interspecific differences

Abstract

Molecular research based on gene sequence analysis and performed for decades, in general, supported morphology-based groupings of the species within the family Culicidae, but phylogenetic relationships between some genera and tribes remained uncertain for a long time. Interspecific differences in catalase, an antioxidant enzyme important for maintaining prolonged lifespan and reproduction, have not been studied extensively by estimating enzymatic activity levels. Here, catalase enzymatic activity was assayed in extracts of male mosquitoes belonging to 10 species of the subfamily Culicinae, including species from tribes of disputable phylogeny. Three species of Chaoboridae (nearest outgroup taxon) and mosquitoes from the subfamily Anophelinae (one species complex) were also added to the study. At least in Culicinae, immature adult males (less than one day after emergence) have distinctly elevated specific activity of catalase; therefore, only mature males of all species were used for the comparative study. As a result, significant differences in catalase activity were revealed between tribes, genera and particular species. Among culicids, the genera Coquillettidia and Culiseta were found to include the species with the highest and relatively high catalase activity, which is consistent with the affinity of the tribes Mansoniini and Culisetini to each other. Within Ochlerotatus, extremely low catalase activity in Oc. hexodontus suggests the more distant position of this species from Oc. cantans (Meigen) and Oc. communis (de Geer) than the positions of the latter two species from each other. Additional study of catalase activity in overwintering females of the genus Culex revealed significantly higher enzyme activity in Cx. torrentium in comparison with Cx. pipiens, which supports their quite distant positions from each other within the genus. Considering the distribution of catalase activity within the tree obtained, the preliminary outcome is that Culiseta retains the elevated level of catalase activity that was lost during the early separation of Anopheles and subsequent separation of Culex and Aedes/Ochlerotatus after Anopheles from their common branch with Culiseta/Coquillettidia. Overall, the use of taxonomic distribution of catalase activity levels appears to be effective for resolving disputed events of mosquito phylogeny.

 

References

  1. Anisimova, M., Gil, M., Dufayard, J.F., Dessimoz, C. & Gascuel, O. (2011) Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Systematic Biology, 60 (5), 685–699. https://doi.org/10.1093/sysbio/syr041
  2. Becker, N., Jöst, A. & Weitzel, T. (2012) The Culex pipiens complex in Europe. Journal of the American Mosquito Control Association, 28 (4s), 53–67. https://doi.org/10.2987/8756-971X-28.4s.53
  3. Becker, N., Petrić, D., Zgomba, M., Boase, C., Madon, M., Dahl, C. & Kaiser, A. (2020) Mosquitoes: identification, ecology and control. 3rd Edition. Springer Nature Switzerland AG, Cham, xxxi + 570 pp. https://doi.org/10.1007/978-3-030-11623-1
  4. Besansky, N.J. & Fahey, G.T. (1997) Utility of the white gene in estimating phylogenetic relationships among mosquitoes (Diptera: Culicidae). Molecular Biology and Evolution, 14 (4), 442–454. https://doi.org/10.1093/oxfordjournals.molbev.a025780
  5. Börstler, J., Lühken, R., Rudolf, M., Steinke, S., Melaun, C., Becker, S., Garms, R. & Krüger, A. (2014) The use of morphometric wing characters to discriminate female Culex pipiens and Culex torrentium. Journal of Vector Ecology, 39 (1), 204–212. https://doi.org/10.1111/j.1948-7134.2014.12088.x
  6. Chen, D.-H., He, S.-L., Fu, W.-B., Yan, Z.-T., Hu, Y.-J., Yuan, H., Wang, M.-B. & Chen, B. (2023) Mitogenome-based phylogeny of mosquitoes (Diptera: Culicidae). Insect Science. [preprint] https://doi.org/10.1111/1744-7917.13251
  7. Chmelová, Ľ., Bianchi, C., Albanaz, A.T., Režnarová, J., Wheeler, R., Kostygov, A.Y., Kraeva, N. & Yurchenko, V. (2021) Comparative analysis of three trypanosomatid catalases of different origin. Antioxidants, 11 (1), 46. https://doi.org/10.3390/antiox11010046
  8. Сое, R.L., Freeman, P. & Mattingly, P.F. (1950) Handbooks for the identification of British insects. Diptera 2, Nematocera: families Tipulidae to Chironomidae. Royal Entomological Society of London, London, 216 pp.
  9. Ganyukova, A.I., Zolotarev, A.V., Malysheva, M.N. & Frolov, A.O. (2018) First record of Trypanosoma theileri-like flagellates in horseflies from Northwest Russia. Protistology, 12 (4), 223–230. https://doi.org/10.21685/1680-0826-2018-12-4-6
  10. Grant, B.J., Rodrigues, A.P., ElSawy, K.M., McCammon, J.A. & Caves, L.S. (2006) Bio3d: an R package for the comparative analysis of protein structures. Bioinformatics, 22 (21), 2695–2696. https://doi.org/10.1093/bioinformatics/btl461
  11. Gutsevich, A.V., Monchadsky, A.S., Shtakelberg, A.A. (1970) Komary. Semeistvo Culicidae. Fauna SSSR. Nasekomye dvukrylye. Nauka, Leningrad, 384 pp. [in Russian]
  12. Harbach, R.E. (2007) The Culicidae (Diptera): a review of taxonomy, classification and phylogeny. Zootaxa, 1668 (1), 591–638. https://doi.org/10.11646/zootaxa.1668.1.28
  13. Harbach, R.E. & Kitching, I.J. (1998) Phylogeny and classification of the Culicidae (Diptera). Systematic Entomology, 23 (4), 327‒370. https://doi.org/10.1046/j.1365-3113.1998.00072.x
  14. Hesson, J.C., Rettich, F., Merdic, E., Vignjevic, G., Ostman, O., Schäfer, M., Schaffner, F., Foussadier, R., Besnard, G., Medlock, J., Scholte, E.J. & Lundström, J.O. (2014) The arbovirus vector Culex torrentium is more prevalent than Culex pipiens in northern and central Europe. Medical and Veterinary Entomology, 28 (2), 179–186. https://doi.org/10.1111/mve.12024
  15. Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35 (2), 518–522. https://doi.org/10.1093/molbev/msx281
  16. Isoe, J. (2000) Comparative analysis of the vitellogenin genes of the Culicidae. PhD Thesis, Faculty of the Interdisciplinary Program in Insect Science, University of Arizona, Tucson, Arizona, 203 pp.
  17. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14 (6), 587–589. https://doi.org/10.1038/nmeth.4285
  18. Karakus, Y.Y. (2020) Typical catalases: function and structure. In: Bagatini, M.D. (Ed.), Glutathione System and Oxidative Stress in Health and Disease. IntechOpen, London, pp. 111–126. https://doi.org/10.5772/intechopen.90048
  19. Kass, R.E. & Raftery, A.E. (1995) Bayes factors. Journal of the American Statistical Association, 90 (430), 773–795. https://doi.org/10.1080/01621459.1995.10476572
  20. Klink, A. (1982) Description of Mochlonyx triangularis n. sp. and a key to the larvae, pupae and imagines of the palearctic species of Mochlonyx Loew (Diptera: Chaoboridae). Entomologische Berichten, 42 (10), 150–155.
  21. Lai, J., Jin, J., Kubelka, J. & Liberles, D.A. (2012) A phylogenetic analysis of normal modes evolution in enzymes and its relationship to enzyme function. Journal of Molecular Biology, 422 (3), 442–459. https://doi.org/10.1016/j.jmb.2012.05.028
  22. Lorenz, C., Alves, J.M., Foster, P.G., Suesdek, L. & Sallum, M.A.M. (2021) Phylogeny and temporal diversification of mosquitoes (Diptera: Culicidae) with an emphasis on the Neotropical fauna. Systematic Entomology, 46 (4), 798–811. https://doi.org/10.1111/syen.12489
  23. Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 193 (1), 265–275. https://doi.org/10.1016/S0021-9258(19)52451-6
  24. Madeira, F., Pearce, M., Tivey, A.R., Basutkar, P., Lee, J., Edbali, O., Madhusoodanan, N., Kolesnikov, A. & Lopez, R. (2022) Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Research, 50 (W1), W276–W279. https://doi.org/10.1093/nar/gkac240
  25. Maté, M.J., Murshudov, G., Bravo, J., Melik-Adamyan, W., Loewen, P.С. & Fita, I. (2001) Heme-catalases. In: Messerschmidt, A., Huber, R., Poulos, T. & Wieghardt, K. (Eds.), Handbook of Metalloproteins. Wiley & Sons, Chichester, pp. 1–18. Available at http://www.loewenlabs.com/peter/wp-content/themes/atahualpa/Manuscripts/hm_01.pdf (accessed 24 October 2021)
  26. Morey, R.D., Rouder, J.N., Jamil, T., Urbanek, S., Forner, K. & Ly, A. (2014) BayesFactor: computation of Bayes factors for common designs. Available at: https://cran.r-project.org/src/contrib/Archive/BayesFactor/ (accessed 31 December 2021)
  27. Munoz-Munoz, J.L., García-Molina, F., Varón, R., Tudela, J., García-Cánovas, F. & Rodríguez-López, J.N. (2009) Generation of hydrogen peroxide in the melanin biosynthesis pathway. Biochimica et Biophysica Acta (BBA)–Proteins and Proteomics, 1794 (7), 1017–1029. https://doi.org/10.1016/j.bbapap.2009.04.002
  28. Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32 (1), 268–274. https://doi.org/10.1093/molbev/msu300
  29. O’Connor, C.T. (1958) The life history and economic importance of Mochlonyx cinctipes (Coquillett) (Diptera: Culicidae). Dissertation, Ohio State University, Columbus, Ohio, 89 pp.
  30. Oliveira, J.H.M., Talyuli, O.A., Goncalves, R.L., Paiva-Silva, G.O., Sorgine, M.H.F., Alvarenga, P.H. & Oliveira, P.L. (2017) Catalase protects Aedes aegypti from oxidative stress and increases midgut infection prevalence of Dengue but not Zika. PLoS Neglected Tropical Diseases, 11 (4), e0005525. https://doi.org/10.1371/journal.pntd.0005525
  31. Paradis, E., Claude, J. & Strimmer, K. (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20 (2), 289–290. https://doi.org/10.1093/bioinformatics/btg412
  32. R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from: http://www.r-project.org/ (accessed 23 July 2022)
  33. Rambaut, A. (2018) FigTree, a graphical viewer of phylogenetic trees. Version 1.4.4. Available from: http://tree.bio.ed.ac.uk/software/figtree (accessed 19 April 2022)
  34. Razygraev, A.V. (2020) A comparative study of catalase activity in Culiseta annulata (Schrank) and Culex pipiens L. (Diptera, Culicidae). Entomological Review, 100 (2), 162–169. https://doi.org/10.1134/S0013873820020037
  35. Razygraev, A.V. (2021) A method for measuring catalase activity in mosquitoes by using ammonium molybdate and reaction medium buffered with 3-(N-morpholino)propanesulfonic acid. Parazitologiya, 55 (4), 318–336. [in Russian] https://doi.org/10.31857/S0031184721040049
  36. Razygraev, A.V. (2022) Activity of catalase in overwintering females of mosquitoes Culex pipiens, Culex torrentium, and Anopheles maculipennis s.l. (Diptera: Culicidae). Proceedings of the Zoological Institute RAS, 326 (4), 294–302. [in Russian] https://doi.org/10.31610/trudyzin/2022.326.4.294
  37. Razygraev, A.V. & Sulesco, T.M. (2020) The use of the Bayes factor for identification of Culex pipiens and C. torrentium (Diptera: Culicidae) based on morphometric wing characters. Entomological Review, 100 (2), 220–227. https://doi.org/10.1134/S0013873820020104
  38. Razygraev, A.V., Yushina, A.D. & Titovich, I.A. (2018) Correction to: a method of measuring glutathione peroxidase activity in murine brain: application in pharmacological experiment. Bulletin of Experimental Biology and Medicine, 165, 589–592. https://doi.org/10.1007/s10517-018-4219-2
  39. Reidenbach, K.R., Cook, S., Bertone, M.A., Harbach, R.E., Wiegmann, B.M. & Besansky, N.J. (2009) Phylogenetic analysis and temporal diversification of mosquitoes (Diptera: Culicidae) based on nuclear genes and morphology. BMC Evolutionary Biology, 9, 298. https://doi.org/10.1186/1471-2148-9-298
  40. Revell, L.J. (2013) Two new graphical methods for mapping trait evolution on phylogenies. Methods in Ecology and Evolution, 4 (8), 754–759. https://doi.org/10.1111/2041-210X.12066
  41. Rezende, E.L. & Diniz‐Filho, J.A.F. (2011) Phylogenetic analyses: comparing species to infer adaptations and physiological mechanisms. Comprehensive Physiology, 2 (1), 639–674. https://doi.org/10.1002/cphy.c100079
  42. Salmela, J., Härmä, O. & Taylor, D.J. (2021) Chaoborus flavicans Meigen (Diptera, Chaoboridae) is a complex of lake and pond dwelling species: a revision. Zootaxa, 4927 (2), 151–196. https://doi.org/10.11646/zootaxa.4927.2.1
  43. Scheckhuber, C.Q. (2015) Arg354 in the catalytic centre of bovine liver catalase is protected from methylglyoxal-mediated glycation. BMC Research Notes, 8, 830. https://doi.org/10.1186/s13104-015-1793-5
  44. Shepard, J.J., Andreadis, T.G. & Vossbrinck, C.R. (2006) Molecular phylogeny and evolutionary relationships among mosquitoes (Diptera: Culicidae) from the northeastern United States based on small subunit ribosomal DNA (18S rDNA) sequences. Journal of Medical Entomology, 43 (3), 443–454. https://doi.org/10.1093/jmedent/43.3.443
  45. Shimodaira, H. & Hasegawa, M. (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution, 16 (8), 1114. https://doi.org/10.1093/oxfordjournals.molbev.a026201
  46. Sim, C. & Denlinger, D.L. (2011) Catalase and superoxide dismutase-2 enhance survival and protect ovaries during overwintering diapause in the mosquito Culex pipiens. Journal of Insect Physiology, 57 (5), 628–634. https://doi.org/10.1016/j.jinsphys.2011.01.012
  47. Sirivanakarn, S. (1976) Medical entomology studies III. A revision of the subgenus Culex in the Oriental region (Diptera: Culicidae). Contributions of the American Entomological Institute, 12 (2), i–iii + 1–271.
  48. Soghigian, J., Sither, C., Justi, S., Morinaga, G., Cassel, B., Vitek, C., Livdahl, T., Xia, S., Gloria-Soria, A., Powell, J., Zavortink, T., Hardy, C., Burkett-Cadena, N., Reeves, L., Wilkerson, R., Dunn, R., Yeates, D., Sallum, M.A., Byrd, B., Trautwein, M., Linton, Y.-M., Reiskind, M. & Wiegmann, B. (2023) An enduring enemy: phylogenomics reveals the history of host use in mosquitoes. Research Square. [preprint] https://doi.org/10.21203/rs.3.rs-2515328/v1
  49. Vanderheyden, A., Smitz, N., De Wolf, K., Deblauwe, I., Dekoninck, W., Meganck, K., Gombeer, S., Vanslembrouck, A., De Witte, J., Schneider, A., Verlé, I., De Meyer, M., Backeljau, T., Müller, R. & Van Bortel, W. (2022) DNA Identification and diversity of the vector mosquitoes Culex pipiens s.s. and Culex torrentium in Belgium (Diptera: Culicidae). Diversity, 14, 486. https://doi.org/10.3390/d14060486
  50. Vera, J.C. (1988) Measurement of microgram quantities of protein by a generally applicable turbidimetric procedure. Analytical Biochemistry, 174 (1), 187–196. https://doi.org/10.1016/0003-2697(88)90534-9
  51. Wilkerson, R.C., Linton, Y.-M. & Strickman, D. (2021) Mosquitoes of the World. Vols. 1 & 2. Johns Hopkins University Press, Baltimore, Maryland, 1332 pp. https://doi.org/10.1186/s13071-021-04848-6
  52. Zámocký, M. & Koller, F. (1999) Understanding the structure and function of catalases: clues from molecular evolution and in vitro mutagenesis. Progress in Biophysics and Molecular Biology, 72 (1), 19–66. https://doi.org/10.1016/S0079-6107(98)00058-3