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Variation in bacterial endosymbionts associated with the date palm hopper, Ommatissus lybicus populations

Published online by Cambridge University Press:  15 August 2017

S. Karimi ,
H. Izadi ,
M. Askari Seyahooei ,
A. Bagheri  and
P. Khodaygan
S. Karimi*
Affiliation:
Department of Plant Protection, Faculty of Agriculture, Vali-e-Asr University, Rafsanjan, Iran
H. Izadi
Affiliation:
Department of Plant Protection, Faculty of Agriculture, Vali-e-Asr University, Rafsanjan, Iran
M. Askari Seyahooei
Affiliation:
Plant Protection Research Department, Hormozgan Agricultural and Natural Resources Research and Education Center, Agricultural Research Education and Extension Organization (AREEO), Bandar Abbas, Iran
A. Bagheri
Affiliation:
Plant Protection Research Department, Hormozgan Agricultural and Natural Resources Research and Education Center, Agricultural Research Education and Extension Organization (AREEO), Bandar Abbas, Iran
P. Khodaygan
Affiliation:
Department of Plant Protection, Faculty of Agriculture, Vali-e-Asr University, Rafsanjan, Iran
*
*Author for correspondence Phone: +98 34 31312156 Fax: +98 34 31312155 E-mail: [email protected]
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Abstract

The date palm hopper, Ommatissus lybicus, is a key pest of the date palm, which is expected to be comprised of many allopatric populations. The current study was carried out to determine bacterial endosymbiont diversity in the different populations of this pest. Ten date palm hopper populations were collected from the main date palm growing regions in Iran and an additional four samples from Pakistan, Oman, Egypt and Tunisia for detection of primary and secondary endosymbionts using polymerase chain reaction (PCR) assay with their specific primers. The PCR products were directly sequenced and edited using SeqMan software. The consensus sequences were subjected to a BLAST similarity search. The results revealed the presence of ‘Candidatus Sulcia muelleri’ (primary endosymbiont) and Wolbachia, Arsenophonus and Enterobacter (secondary endosymbionts) in all populations. This assay failed to detect ‘Candidatus Nasuia deltocephalinicola’ and Serratia in these populations. ‘Ca. S. muelleri’ exhibited a 100% infection frequency in populations and Wolbachia, Arsenophonus and Enterobacter demonstrated 100, 93.04 and 97.39% infection frequencies, respectively. The infection rate of Arsenophonus and Enterobacter ranged from 75 to 100% and 62.5 to 100%, respectively, in different populations of the insect. The results demonstrated multiple infections by ‘Ca. Sulcia muelleri’, Wolbachia, Arsenophonus and Enterobacter in the populations and may suggest significant roles for these endosymbionts on date palm hopper population fitness. This study provides an insight to endosymbiont variation in the date palm hopper populations; however, further investigation is needed to examine how these endosymbionts may affect host fitness.

Keywords

Arsenophonusbacterial endosymbiontEnterobacterOmmatissus lybicusSulciaWolbachia
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 2 , April 2018 , pp. 271 - 281
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Copyright
Copyright © Cambridge University Press 2017 

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References

Ali, A.S.A. (2011) Influence of climatic factors on the recent spread of dubas bug Ommatissus lybicus (Debergevin) on date palm trees in some upper euphrates regions of al-anbar province. Journal of Agricultural Science and Technology 1, 544–549.Google Scholar
Barr, K.L., Hearne, L.B., Briesacher, S., Clark, T.L. & Davis, G.E. (2010) Microbial symbionts in insects influence down-regulation of defense genes in maize. PLoS ONE 5, e11339.Google ScholarPubMed
Ben-Yosef, M., Jurkevitch, E. & Yuval, B. (2008) Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata . Physiological Entomology 33, 145–154.Google Scholar
Bressan, A. (2014) Emergence and evolution of Arsenophonus bacteria as insect-vectored plant pathogens. Infection, Genetics and Evolution 22, 81–90.CrossRefGoogle ScholarPubMed
Bressan, A., Arneodo, J., Simonato, M., Haines, W.P. & Boudon-Padieu, E. (2009) Characterization and evolution of two bacteriome-inhabiting symbionts in cixiid planthoppers (Hemiptera: Fulgoromorpha: Pentastirini). Environmental Microbiology 11, 3265–3279.CrossRefGoogle ScholarPubMed
Bressan, A., Terlizzi, F. & Credi, R. (2012) Independent origins of vectored plant pathogenic bacteria from arthropod-associated Arsenophonus endosymbionts. Microbial Ecology 63, 628–638.Google Scholar
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, 407–413.CrossRefGoogle ScholarPubMed
de Leon, J.H., Jones, W.A., Setamou, M. & Morgan, D.J. (2006) Genetic and hybridization evidence confirms that a geographic population of Gonatocerus morrilli (Hymenoptera: Mymaridae) from California is a new species: Egg parasitoids of the glassy-winged sharpshooter Homalodisca coagulata (Homoptera: Cicadellidae). Biological control 36, 282–293.CrossRefGoogle Scholar
Dohlen, C.D., Spaulding, U., Shields, K., Havill, N.P., Rosa, C. & Hoover, K. (2013) Diversity of proteobacterial endosymbionts in hemlock woolly adelgid (Adelges tsugae) (Hemiptera: Adelgidae) from its native and introduced range. Environmental Microbiology 15, 2043–2062.Google Scholar
Douglas, A.E. (2007) Symbiotic microorganisms: untapped resources for insect pest control. Trends in Biotechnology 25, 338–342.Google Scholar
Douglas, A.E., Francois, C.L.M.J. & Minto, L.B. (2006) Facultative ‘secondary’ bacterial symbionts and the nutrition of the pea aphid, Acyrthosiphon pisum . Physiological Entomology 31, 262–269.Google Scholar
Duron, O., Schneppat, U.E., Berthomieu, A., Goodman, S.M., Droz, B., Paupy, C., Nkoghe, J.O., Rahola, N. & Tortosa, P. (2014) Origin, acquisition and diversification of heritable bacterial endosymbionts in louse flies and bat flies. Molecular Ecology 23, 2105–2117.Google Scholar
Fukatsu, T. and Nikoh, N. (1998) Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Applied Environnmental Microbiology 64, 3599–3606.CrossRefGoogle ScholarPubMed
Gherna, R.L., Werren, J.H., Weisburg, W., Cote, R., Woese, C.R., Mandelco, L. & Brenner, D.J. (1991) Arsenophonus nasoniae gen. nov., sp. nov., the causative agent of the son-killer trait in the parasitic wasp Nasonia vitripennis . International Journal of Systematic and Evolutionary Microbiology 41, 563–565.Google Scholar
Hamilton, P.T. & Perlman, S.J. (2013) Host defense via symbiosis in Drosophila . PLoS Pathogens 9, e1003808.Google Scholar
Hansen, A.K. & Moran, N.A. (2014) The impact of microbial symbionts on host plant utilization by herbivorous insects. Molecular Ecology 23, 1473–1496.Google Scholar
Hansen, A.K., Jeong, G., Paine, T.D. & Stouthamer, R. (2007) Frequency of secondary symbiont infection in an invasive psyllid relates to parasitism pressure on a geographic scale in California. Applied and Environmental Microbiology 73, 7531–7535.Google Scholar
Hong-Xing, X., Xu-Song, Z., Ya-Jun, Y., Jun-Ce, T., Qiang, F., Gong-Yin, Y. & Zhong-Xian, L. (2015) Changes in endosymbiotic bacteria of brown planthoppers during the process of adaptation to different resistant rice varieties. Environmental Entomology 44, 582–587.CrossRefGoogle ScholarPubMed
Howard, F.W. (2001) Sap-feeders on palms. pp. 109–232 in Howard, F.W., Moore, D., Giblin-Davis, R.M. & Abad, R.G. (Ed.) Insects on Palms. Wallingford, CABI Publishing.Google Scholar
Hussain, A.A. (1963) Biology and control of the dubas bug, Ommatissus binotatus lybicus De Berg.(Homoptera, Tropiduchidae), infesting date palms in Iraq. Bulletin of Entomological Research 53, 737–745.Google Scholar
Indiragandhi, P., Yoon, C., Yang, J.O., Cho, S., Sa, T.M. & Kim, G.H. (2010) Microbial communities in the developmental stages of B and Q biotypes of sweetpotato whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). Journal of Applied Biological Chemistry 53, 605–617.Google Scholar
Ishii, Y., Matsuura, Y., Kakizawa, S., Nikoh, N. & Fukatsu, T. (2013) Diversity of bacterial endosymbionts associated with Macrosteles leafhoppers vectoring phytopathogenic phytoplasmas. Applied and Environmental Microbiology 79, 5013–5022.Google Scholar
Jeyaprakash, A. & Hoy, M.A. (2010) Real-time PCR reveals endosymbiont titer fluctuations in Metaseiulus occidentalis (Acari: Phytoseiidae) colonies held at different temperatures. Florida Entomologist 93, 464–466.Google Scholar
Jousselin, E., Coeur d'Acier, A., Vanlerberghe-Masutti, F. & Duron, O. (2013) Evolution and diversity of Arsenophonus endosymbionts in aphids. Molecular Ecology 22, 260–270.Google Scholar
Kobialka, M., Michalik, A., Walczak, M., Junkiert, L. & Szklarzewicz, T. (2016) Sulcia symbiont of the leafhopper Macrosteles laevis (Ribaut, 1927) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae) harbors Arsenophonus bacteria. Protoplasma 253, 903–912.Google Scholar
Koga, R., Bennett, G.M., Cryan, J.R. & Moran, N.A. (2013) Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage. Environmental Microbiology 15, 2073–2081.Google Scholar
Lauzon, C.R., Sjogren, R.E. & Prokopy, R.J. (2000) Enzymatic capabilities of bacteria associated with apple maggot flies: a postulated role in attraction. Journal of Chemical Ecology 26, 953–967.CrossRefGoogle Scholar
Liu, L.J., Martinez-Sañudo, I., Mazzon, L., Prabhakar, C.S., Girolami, V., Deng, Y.L., Dai, Y. & Li, Z.H. (2016) Bacterial communities associated with invasive populations of Bactrocera dorsalis (Diptera: Tephritidae) in China. Bulletin of Entomological Research 106, 718–728.Google Scholar
Liu, Y.K. (2011). Comparative studies on host fitness, defensive enzymes and symbionts of the three rice planthoppers. Chinese Academy of Agricultural Sciences Dissertation.Google Scholar
Matsuura, Y., Kikuchi, Y., Hosokawa, T., Koga, R., Meng, X.Y., Kamagata, Y., Nikoh, N. & Fukatsu, T. (2012) Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs. ISME Journal 6(2), 397–409.Google Scholar
McCutcheon, J.P. & Moran, N.A. (2010) Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biology and Evolution 2, 708–718.Google Scholar
McCutcheon, J.P., McDonald, B.R. & Moran, N.A. (2009) Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proceedings of the National Academy of Sciences 106, 15394–15399.Google Scholar
Michalik, A., Jankowska, W., Kot, M., Gołas, A. & Szklarzewicz, T. (2014) Symbiosis in the green leafhopper, Cicadella viridis (Hemiptera, Cicadellidae). Association in statu nascendi? Arthropod Structure and Development 43, 579–587.Google Scholar
Moran, N.A., Tran, P. & Gerardo, N.M. (2005) Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Applied and Environmental Microbiology 71, 8802–8810.Google Scholar
Moss, M. (2002) Bacterial pigments. Microbiologist 3, 10–12.Google Scholar
Müller, H.J. (1940) Die symbiose der fulgoroiden (Homoptera: Cicadina). Zoologica 98, 1–110, 111–220.Google Scholar
Müller, H.J. (1962) Neuere vorstellungen über verbreitung und phylogenie der endosymbiosen der zikaden. Zeitschrift für Morphologie und Ökologie der Tiere 51, 190–210.Google Scholar
Noda, H., Watanabe, K., Kawai, S., Yukuhiro, F., Miyoshi, T., Tomizawa, M., Koizumi, Y., Nikoh, N. & Fukatsu, T. (2012) Bacteriome-associated endosymbionts of the green rice leafhopper Nephotettix cincticeps (Hemiptera: Cicadellidae). Applied Entomology and Zoology 47, 217–225.Google Scholar
Nováková, E., Husník, F., Šochová, E. & Hypša, V. (2015) Arsenophonus and Sodalis symbionts in louse flies: an analogy to the Wigglesworthia and Sodalis system in tsetse flies. Applied and Environmental Microbiology 81, 6189–6199.Google Scholar
Oliver, K.M., Degnan, P.H., Burke, G.R. & Moran, N.A. (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annual Review of Entomology 55, 247–266.Google Scholar
Peloquin, J.J. & Greenberg, L. (2003) Identification of midgut bacteria from fourth instar red imported fire ant larvae, Solenopsis invicta buren (Hymenoptera: Formicidae). Journal of Agricultural and Urban Entomology 20, 157–164.Google Scholar
Perotti, M.A., Allen, J.M., Reed, D.L. & Braig, H.R. (2007) Host-symbiont interactions of the primary endosymbiont of human head and body lice. FASEB Journal 21, 1058–1066.Google Scholar
Qu, L.Y., Lou, Y.H., Fan, H.W., Ye, Y.X., Huang, H.J., Hu, M.Q., Zhu, Y.N. & Zhang, C.X. (2013) Two endosymbiotic bacteria, Wolbachia and Arsenophonus , in the brown planthopper Nilaparvata lugens . Symbiosis 61, 47–53.Google Scholar
Ratzka, C., Gross, R. & Feldhaar, H. (2012) Endosymbiont tolerance and control within insect hosts. Insects 3, 553–572.Google Scholar
Reineke, A., Karlovsky, P. & Zebitz, C.P.W. (1998) Preparation and purification of DNA from insects for AFLP analysis. Insect molecular Biology 7, 95–99.Google Scholar
Ricci, I., Valzano, M., Ulissi, U., Epis, S., Cappelli, A. & Favia, G. (2012) Symbiotic control of mosquito borne disease. Pathogens and Global Health 106, 380–385.Google Scholar
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Russell, J.A., Funaro, C.F., Giraldo, Y.M., Goldman-Huertas, B., Suh, D., Kronauer, D.J., Moreau, C.S. & Pierce, N.E. (2012) A veritable menagerie of heritable bacteria from ants, butterflies, and beyond: broad molecular surveys and a systematic review. PLoS ONE 7, e51027.Google Scholar
Sacchi, L., Genchi, M., Clementi, E., Bigliardi, E., Avanzati, A.M., Pajoro, M., Negri, I., Marzorati, M., Gonella, E., Alma, A. & Daffonchio, D. (2008) Multiple symbiosis in the leafhopper Scaphoideus titanus (Hemiptera: Cicadellidae): details of transovarial transmission of Cardinium sp. and yeast-like endosymbionts. Tissue and Cell 40, 231–242.Google Scholar
Singh, S.T., Priya, N.G., Kumar, J., Rana, V.S., Ellango, R., Joshi, A., Priyadarshini, G., Asokan, R. & Rajagopal, R. (2012) Diversity and phylogenetic analysis of endosymbiotic bacteria from field caught Bemisia tabaci from different locations of North India based on 16S rDNA library screening. Infection, Genetics and Evolution 12, 411–419.Google Scholar
Takiya, D.M., Tran, P.L., Dietrich, H. & Moran, N.A. (2006) Co-cladogenesis spanning three phyla: leafhoppers (Insecta: Hemiptera: Cicadellidae) and their dual bacterial symbionts. Molecular Ecology 15, 4175–4191.Google Scholar
Taylor, G.P., Coghlin, P.C., Floate, K.D. & Perlman, S.J. (2011) The host range of the male-killing symbiont Arsenophonus nasoniae in filth fly parasitioids. Journal of Invertebrate Pathology 106, 371–379.Google Scholar
Trowbridge, R.E., Dittmar, K. & Whiting, M.F. (2006) Identification and phylogenetic analysis of Arsenophonus- and Photorhabdus-type bacteria from adult Hippoboscidae and Streblidae (Hippoboscoidea). Journal of Invertebrate Pathology 91, 64–68.Google Scholar
Tsuchida, T., Koga, R., Shibao, H., Matsumoto, T. & Fukatsu, T. (2002) Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum . Molecular Ecology 11, 2123–2135.Google Scholar
Tsuchida, T., Koga, R., Fujiwara, A. & Fukatsu, T. (2014) Phenotypic effect of ‘Candidatus Rickettsiella viridis,’ a facultative symbiont of the pea aphid (Acyrthosiphon pisum), and its interaction with a coexisting symbiont. Applied and Environmental Microbiology 80, 525–533.Google Scholar
Urban, J.M. & Cryan, J.R. (2012) Two ancient bacterial endosymbionts have coevolved with the planthoppers (Insecta: Hemiptera: Fulgoroidea). BMC Evolutionary Biology 12, 1.Google Scholar
Wang, J., Chung, S.H., Peiffer, M., Rosa, C., Hoover, K., Zeng, R. & Felton, G.W. (2016) Herbivore oral secreted bacteriat distinct defense responses in preferred and non-preferred host plants. Journal of Chemical Ecology 42, 463–474.Google Scholar
Wang, W.X., Zhu, T.H., Lai, F.X. & Fu, Q. (2015) Diversity and infection frequency of symbiotic bacteria in different populations of the rice brown planthopper in China. Journal of Entomological Science 50, 47–66.Google Scholar
Wangkeeree, J., Miller, T.A. & Hanboonsong, Y. (2012) Candidates for symbiotic control of sugarcane white leaf disease. Applied and Environmental Microbiology 78, 6804–6811.Google Scholar
Werren, J.H., Baldo, L. & Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology 6, 741–751.Google Scholar
White, J.A., Giorgini, M., Strand, M.R. & Pennacchio, F. (2013) Arthropod endosymbiosis and evolution. pp. 441–477 in Minelli, A., Boxshall, G. & Fusco, G. (Ed.) Arthropod Biology and Evolution. Berlin, Heidelberg, Germany, Springer.Google Scholar
Xu, H.X., Zheng, X.S., Yang, Y.J., Xin, W., Ye, G.Y. and Lu, Z.X. (2014) Bacterial community in different populations of rice brown planthopper Nilaparvata lugens (Stål). Rice Science 21, 59–64.Google Scholar
Xue, X., Li, S.J., Ahmed, M.Z., De Barro, P.J., Ren, S.X. and Qiu, B.L. (2012) Inactivation of Wolbachia reveals its biological roles in whitefly host. PLoS ONE 7, e48148.Google Scholar
Zhou, W., Rousset, F. and O'Neill, S. (1998) Phylogeny and PCR-based classification of strains using wsp gene sequences. Proceedings of the Royal Society of London B: Biological Sciences 265, 509–515.Google Scholar