Diversity and prevalence of endosymbionts in populations of the two-spotted spider mite on different plant hosts in North, Razavi, and South Khorasan Provinces, Iran, and the effect of temperature on the vertical transmission of symbiotic bacteria

Authors

1 Ferdowsi University of Mashhad

2 Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, Iran

Abstract
Many bacteria associated with arthropods play important roles in host functional traits, and the structure of these bacteria can be influenced by intracellular symbionts. In this study, a survey of bacterial endosymbionts present in natural populations of the two-spotted spider mite, Tetranychus urticae, was conducted in North, Razavi, and South Khorasan Provinces. A total of 1440 spider mites collected from three localities associated with eight host plants were screened for endosymbionts. Among the three detected facultative endosymbionts, Wolbachia, Cardinium, and Rikettsia, different infection frequencies (91.6%, 9.72%, and 9.72%, respect-ively) were observed. None of the individuals carried Arsenophonus or Spiroplasma. In the majority of the studied populations, multiple infections by endosymbiont were detected and the prevalence of individuals with the Wolbachia-Rikettsia coinfection (9.72%) was higher than the frequency of the individual coinfection rates with other symbionts. The findings of the current study suggest that the frequencies of endosymbiont infections may be affected by collection site characteristics, including geographic location (latitude, longitude), altitude, and collection date, as well as host plant species. Wolbachia infection rates were higher in mites collected from Razavi Khorasan Province compared to those from other localities. The highest frequencies of Cardinium and Rickettsia were observed in North and South Khorasan Provinces. Host plants also significantly influenced the prevalence of endosymbionts in the present study. The results of vertical transmission experiments indicated that temperature influences vertical transmission in symbiotic bacteria.

Keywords


Breeuwer, J.A. & Jacobs, G. (1996) Wolbachia: intercellular manipulators of mite reproduction. Experi-mental and Applied Acarology, 20(8): 421–434.
Chiel, E., Gottlieb, Y., Zchori-Fein, E., Mozes-Daube, N., Katzir, N., Inbar, M. & Ghanim, M. (2007) Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bulletin of Entomological Research, 97(4): 407–413.
Clancy, D.J. & Hoffmann, A.A. (1998) Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia‐infected Drosophila simulans. Entomologia Experimentalis et Applicata, 86(1): 13–24.
Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7: 214. https://doi.org/10.1186/1471-2148-7-214
Duron, O., Bouchon, D., Boutin, S., Bellamy. L., Zhou, L., Engelstädter, J. & Hurst, G.D. (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biology, 6: 1–12.
Enigl, M. & Schausberger, P. (2007) Incidence of the endosymbionts Wolbachia, Cardinium and Spiroplasma in phytoseiid mites and associated prey. Experimental and Applied Acarology, 42:75–85.
Famah Sourassou, N., Hanna, R., Breeuwer, J.A., Negloh, K., de Moraes, G.J. & Sabelis, M.W. (2014) The endosymbionts Wolbachia and Cardinium and their effects in three populations of the predatory mite Neoseiulus paspalivorus. Experimental and Applied Acarology, 64(2): 207–221.
Ferrari, J. & Vavre, F. (2011) Bacterial symbionts in insects or the story of communities affecting communities. Philosophical Transactions of the Royal Society B: Biological Sciences, 366(1569): 1389–1400. https://doi.org/10.1098/rstb.2010.0226
Floate, KD., Kyei-Poku, G.K. & Coghlin, P.C. (2006) Overview and relevance of Wolbachia bacteria in biocontrol research. Biocontrol Science and Technology ,16(8): 767–788.
Fukatsu, T. and Nikoh, N. (1998) Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Applied and Environmental Microbiology, 64(10): 3599–3606.
Fukatsu, T., Tsuchida, T., Nikoh, N. & Koga, R. (2001) Spiroplasma symbiont of the pea aphid, Acyrthosiphon pisum (Insecta: Homoptera). Applied and Environmental Microbiology, 67(3): 1284–1291.
Gotoh, T., Noda, H. & Hong, X.Y. (2003). Wolbachia distribution and cytoplasmic incompatibility based on a survey of 42 spider mite species (Acari: Tetranychidae) in Japan. Heredity, 91(3): 208–216.
Gotoh, T., Sugasawa, J., Noda., H. & Kitashima, Y. (2007) Wolbachia-induced cytoplasmic incompatibility in Japanese populations of Tetranychus urticae (Acari: Tetranychidae). Experimental and Applied Acarology, 42: 1–16.
Grbić, M., Van Leeuwen, T., Clark, R.M., Rombauts, S., Rouzé, P., Grbić, V., Osborne, E.J., Dermauw, W., Thi Ngoc, P.C., Ortego, F. & Van de Peer, Y. (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature, 479(7374): 487–492.
Gueguen, G., Vavre, F., Gnankine, O., Peterschmitt, M., Charif, D., Chiel, E. & Fleury, F. (2010) Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Molecular Ecology, 19(19): 4365–4376.
Harborne, J.B. (2014) Introduction to ecological biochemistry. Academic Press, London, 336 pp.
Hellard. E., Fouchet, D., Vavre, F. & Pontier, D. (2015) Parasite–parasite interactions in the wild: how to detect them? Trends in Parasitology, 31(12): 640–652.
Jeppson, L.R., Keifer, H.H. & Baker, N.N. (1975) Mites injurious to economic plants. University of California Press, Berkely, 614 pp.
Kashkouli, M., Mehrabadi, M. & Fathipour, Y. (2021) The symbionts. In: Omkar (Ed.), Microbial approaches for insect pest management. Springer, pp. 217–269.
Li, T., Chen, X.L. & Hong, X.Y. (2009) Population genetic structure of Tetranychus urticae and its sibling species Tetranychus cinnabaribus (Acari: Tetranychidae) in China as inferred from microsatellite data. Annals of the Entomological Society of America, 102(4): 674–683.
Liu, Y., Miao, H. & Hong, X.Y. (2006) Distribution of the endosymbiotic bacterium Cardinium in Chinese populations of the carmine spider mite Tetranychus cinnabarinus (Acari: Tetranychidae). Journal of Applied Entomology, 130(9–10): 523–529.
Margolies, D.C. & Wrensch, D.L. (1996) Temperature‐induced changes in spider mite fitness: Offsetting effects of development time, fecundity, and sex ratio. Entomologia Experimentalis et Applicata, 78(1): 111–118.
Migeon, A. & Dorkeld, F. (2020) Spider Mites Web: A comprehensive database for the Tetranychidae. 2006–2020. Institute for Agronomy Research, Center for Biology and Management of Populations: Montpellier, France. Available from: http://www1.montpellier.inra.fr/CBGP/spmweb (Accessed on 2 March 2020).
Nakamura, Y., Kawai, S., Yukuhiro, F., Ito, S., Gotoh, T., Kisimoto, R. & Noda, H. (2009) Prevalence of Cardinium bacteria in planthoppers and spider mites and taxonomic revision of “Candidatus Cardinium hertigii” based on detection of a new Cardinium group from biting midges. Applied and Environmental Microbiology, 75(21): 6757–6763.
Nasehi, S.F., Fathipour, Y., Asgari, S. & Mehrabadi, M. (2022) Environmental temperature, but not male age, affects Wolbachia and prophage WO thereby modulating cytoplasmic incompatibility in the parasitoid wasp, Habrobracon hebetor. Microbial Ecology, 83(2): 482-491.
Rambaut, A. (2008) FigTree v. 1.4.0. Available from http://tree.bio.ed.ac.uk/software/figtree/(Accessed 20 May 2013)
Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, syy032.
Ribeiro, F.R., Vital, C.E., Silva Junior, N.R.D., Barros, R.D.A., da Silva, M.D.C.S., Solís-Vargas, M., Cordeiro, G., da Silva, C.R., Pallini, Â., Ramos, H.J.D.O. & Oliveira, M.G.D.A. (2020) Analysis of the diversity of endosymbiotic microorganisms in two spider mite species. International Journal of Acarology, 46(1): 22–30.
Ros, V.I., Fleming, V.M., Feil, E.J. & Breeuwer, J.A. (2012). Diversity and recombination in Wolbachia and Cardinium from Bryobiaspider mites. BMC Microbiology 12(1): 1–15.
Ross, P.A., Wiwatanaratanabutr, I., Axford, J.K., White, V.L., Endersby-Harshman, N.M. & Hoffmann, A.A. (2017) Wolbachia infections in Aedes aegypti differ markedly in their response to cyclical heat stress. PLOS pathogens, 13(1): e1006006. https://doi.org/10.1371/journal.ppat.1006006
Santamaria, M.E., Arnaiz, A., Rosa-Diaz, I., González-Melendi, P., Romero-Hernandez, G., Ojeda-Martinez, D.A., Garcia, A., Contreras, E., Martinez, M. & Diaz, I. (2020) Plant defenses against Tetranychus urticae: mind the gaps. Plants, 9(4): 464.
Singh, K.S., Troczka, B.J., Duarte, A., Balabanidou, V., Trissi, N., Carabajal Paladino, L.Z., Nguyen, P., Zimmer, C.T., Papapostolou, K.M., Randall, E., Lueke, B., Marec, F., Mazzoni, E., Williamson, M.S., Hayward, A., Nauen, R., Vontas, J. & Bass, C. (2020) The genetic architecture of a host shift: An adaptive walk protected an aphid and its endosymbiont from plant chemical defenses. Science Advances, 6(19): eaba1070.
Stouthamer, R., Breeuwer, JA. & Hurst, G.D. (1999). Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annual Reviews in Microbiology ,53(1); 71–102.
Suchard, M.A., Lemey, P., Baele, G., Ayres, D.L., Drummond, A.J. & Rambaut, A. (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10 Virus Evolution 4: vey016.
Thao, M.L. & Baumann, P. (2004) Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Applied and Environmental Microbiology, 70(6): 3401–3406.
Toju, H. & Fukatsu, T. (2011) Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Molecular Ecology, 20 (4): 853–868.
Van Opijnen, T. & Breeuwer, J.A.J. (1999) High temperatures eliminate Wolbachia, a cytoplasmic incompatibility inducing endosymbiont, from the two-spotted spider mite. Experimental and Applied Acarology, 23(11): 871–881.
Van Leeuwen, T., Tirry, L., Yamamoto, A., Nauen, R. & Dermauw, W. (2015) The economic importance of acaricides in the control of phytophagous mites and an update on recent acaricide mode of action research. Pesticide Biochemistry and Physiology, 121: 12–21.
Vautrin, E. & Vavre, F. (2009) Interactions between vertically transmitted symbionts: cooperation or conflict? Trends in Microbiology, 17(3): 95–99.
Vautrin, E., Genieys, S., Charles, S. & Vavre, F. (2008). Do vertically transmitted symbionts co‐existing in a single host compete or cooperate? A modelling approach. Journal of Evolutionary Biology, 21(1): 145–161.
Weinert, L.A., Araujo-Jnr, E.V., Ahmed, M.Z. & Welch, J.J. (2015) The incidence of bacterial endosym-bionts in terrestrial arthropods. Proceedings of the Royal Society B: Biological Sciences 282(1807): 20150249
Wu, K.E., & Hoy, M.A. (2012) Cardinium is associated with reproductive incompatibility in the predatory mite Metaseiulus occidentalis (Acari: Phytoseiidae). Journal of Invertebrate Pathology, 110(3): 359–365.
Zélé, F., Santos, I., Olivieri, I., Weill, M., Duron, O. & Magalhães, S. (2018) Endosymbiont diversity and prevalence in herbivorous spider mite populations in South-Western Europe. FEMS Microbiology Ecology, 94(4): fiy015. https://doi.org/10.1038/s41437-020-0297-9
Zhang, B., Leonard, S.P., Li, Y. & Moran, N.A. (2019). Obligate bacterial endosymbionts limit thermal tolerance of insect host species. Proceedings of the National Academy of Sciences of the United States of America, 116: 24712–24718. https://doi.org/10.1073/pnas.1915307116
Zhang, Y.C., Cao, W.J., Zhong, L.R., Godfray, H.C.J. & Liu, X.D. (2016a) Host plant determines the population size of an obligate symbiont (Buchnera aphidicola) in aphids. Applied and Environmental Microbiology, 82(8): 2336–2346.
Zhang, Y.K., Chen, Y.T., Yang, K. & Hong, X.-Y. (2016b) A review of prevalence and phylogeny of the bacterial symbiont Cardinium in mites (subclass: Acari). Systematic Applied Acarology, 21: 978–90.
Zhang, Y.K., Chen, Y.T., Yang, K., Qiao, G.X. & Hong, X.Y. (2016c) Screening of spider mites (Acari: Tetranychidae) for reproductive endosymbionts reveals links between co-infection and evolution-ary history. Scientific Reports, 6(1): 1–9.
Zhang, Y.K., Yang, K., Zhu, Y.X. & Hong, X.Y. (2018) Symbiont-conferred reprodution and fitness benefits can favour their host occurrence. Ecology and Evolution, 8(3): 1626–1633.
Zhang, Y.K., Zhang, K.J., Sun, J.T., Yang, X.-M., Ge, C. & Hong, X.-Y. (2013) Diversity of Wolbachia in natural populations of spider mites (genus Tetranychus): Evidence for complex infection history and disequilibrium distribution. Microbial Ecology, 65: 731–739.
Zhao, D.X., Zhang, X.F., & Hong, X. Y. (2013) Host-symbiont interactions in spider mite Tetranychus truncatus doubly infected with Wolbachia and Cardinium. Environmental Entomology, 42(3): 445–452.
Zhou, W., Rousset, F. & O'Neill, S. (1998) Phylogeny and PCR–based classification of Wolbachia strains using wsp gene sequences. Proceedings of the Royal Society of London, Series B: Biological Sciences, 265(1395): 509–515.
Zhu, Y.X., Song, Y.L., Zhang, Y.K., Hoffmann, A.A., Zhou, J.C., Sun, J.T. & Hong, X.Y. (2018) Incidence of facultative bacterial endosymbionts in spider mites associated with local environments and host plants. Applied and Environmental Microbiology, 84(6): e02546-17.