Skip to main content Accessibility help

Diversity and localization of bacterial symbionts in three whitefly species (Hemiptera: Aleyrodidae) from the east coast of the Adriatic Sea

  • M. Škaljac (a1), K. Žanić (a1), S. Hrnčić (a2), S. Radonjić (a2), T. Perović (a3) and M. Ghanim (a4)...


Several whitefly species (Hemiptera: Aleyrodidae) are cosmopolitan phloem-feeders that cause serious damage in numerous agricultural crops. All whitefly species harbor a primary bacterial symbiont and a diverse array of secondary symbionts which may influence several aspects of the insect's biology. We surveyed infections by secondary symbionts in Bemisia tabaci (Gennadius), Trialeurodes vaporariorum (Westwood) and Siphoninus phillyreae (Haliday) from areas in the east cost of the Adriatic Sea. Both the Middle East-Asia Minor 1 (MEAM1) and Mediterranean (MED) B. tabaci genetic groups were detected in Montenegro, whereas only the MED was confirmed in Croatia. Trialeurodes vaporariorum and S. phillyreae were found in all areas surveyed. MEAM1 and MED exhibited similarity to previously reported infections, while populations of T. vaporariorum from Montenegro harbored Rickettsia, Wolbachia and Cardinium in addition to previously reported Hamiltonella and Arsenopnohus. Siphoninus phillyreae harbored Hamiltonella, Wolbachia, Cardinium and Arsenophonus, with the latter appearing in two alleles. Multiple infections of all symbionts were common in the three insect species tested, with some reaching near fixation. Florescent in situ hybridization showed new localization patterns for Hamiltonella in S. phillyreae, and the morphology of the bacteriosome differed from that observed in other whitefly species. Our results show new infections with bacterial symbionts in the whitefly species studied. Infections with the same symbionts in reproductively isolated whitefly species confirm complex relationships between whiteflies and bacterial symbionts, and suggest possible horizontal transfer of some of these bacteria.


Corresponding author

*Author for correspondence Fax: +385 21 31 65 84 E-mail:


Hide All
Aksoy, S., Chen, X. & Hypša, V. (1997) Phylogeny and potential transmission routes of midgut-associated endosymbionts of tsetse (Diptera: Glossinidae). Insect Molecular Biology 6, 183190.
Alemandri, V., De Barro, P., Bejerman, N., Argüello Caro, E.B., Dumon, A.D., Mattio, M.F., Rodriguez, S.M. & Truol, G. (2012) Species Within the Bemisia tabaci (Hemiptera: Aleyrodidae) Complex in Soybean and Bean Crops in Argentina. Journal of Economic Entomology 105, 4853.
Baumann, P. (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annual Review of Microbiology 59, 155189.
Bensadia, F., Boudreault, S., Guay, J.-F., Michaud, D. & Cloutier, C. (2005) Aphid clonal resistance to a parasitoid fails under heat stress. Journal of Insect Physiology 52, 146157.
Boykin, L.M., Shatters, R.G. Jr, Rosell, R.C., McKenzie, C.L., Bagnall, R.A., De Barro, P.J. & Frohlich, D.R. (2007) Global relationships of Bemisia tabaci (Hemiptera: Aleyrodidae) revealed using Bayesian analysis of mitochondrial COI DNA sequences. Molecular Phylogenetics and Evolution 3, 13061319.
Brown, J.K. (2007) The Bemisia tabaci complex: genetic and phenotypic variation and relevance toTYLCV-vector interactions. pp. 2557in Czosnek, H. (Ed.) Tomato Yellow Leaf Curl Virus Disease: Managment, Molecular Biology, Breeding for Resistance. Netherlands, Springer.
Brown, J.K., Frohlich, D.R. & Rosell, R.C. (1995) The sweet-potato or silverleaf whiteflies: biotypes of Bemisia tabaci or a species complex? Annual Review of Entomology 40, 511534.
Brumin, M., Kontsedalov, S. & Ghanim, M. (2011) Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Science 18, 5766.
Buchner, P. (1965) Endosymbiosis of Animals with Plant Microorganisms. New York, USA, John Wiley and Sons.
Caspi-Fluger, A., Inbar, M., Mozes-Daube, N., Katzir, N., Portnoy, V., Belausov, E., Hunter, M.S. & Zchori-Fein, E. (2011) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proceeding of the Royal Society, Series B 279, 17911796.
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, 407413.
Chu, D., Gao, C.S., De Barro, P., Zhang, Y.J., Wan, F.H. & Khan, I.A. (2011) Further insights into the strange role of bacterial endosymbionts in whitefly, Bemisia tabaci: Comparison of secondary symbionts from biotypes B and Q in China. Bulletin of Entomological Research 101, 477486.
Dale, C. & Moran, N.A. (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126(3), 453465.
De Barro, P. & Ahmed, M.Z. (2011) Genetic networking of the Bemisia tabaci cryptic species complex reveals pattern of biological invasions. PLoS ONE 6(10), e25579 (doi:10.1371/journal.pone.0025579).
De Barro, P.J., Scott, K.D., Graham, G.C., Lange, C.L. & Schutze, M.K. (2003) Isolation and characterization of microsatellite loci in Bemisia tabaci. Molecular Ecology Notes 3, 4043.
Dinsdale, A.B., Cook, L., Riginos, C., Buckley, Y.M. & De Barro, P. (2010) Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase I to identify species level genetic boundaries. Annals of the Entomological Society of America 103, 196208.
Dyson, E.A., Kamath, M.K. & Hurst, G.D.D. (2002) Wolbachia infection associated with all-female broods in Hypolimnas bolina (Lepidoptera: Nymphalidae): evidence for horizontal transmission of a butterfly male killer. Heredity 88, 166171.
Everett, K.D.E., Thao, M.L., Horn, M., Dyszynski, G.E. & Baumann, P. (2005) Novel chlamydiae in whiteflies and scale insects: endosymbionts ‘Candidatus Fritschea bemisiae’ strain Falk and ‘Candidatus Fritschea eriococci’ strain Elm. International Journal of Systematic and Evolutionary Microbiology 55, 15811587.
Ferrari, J., Darby, A.C., Daniell, T.J., Godfray, H.C.J. & Douglas, A.E. (2004) Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecological Entomology 29, 6065.
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 Bacteriology 41, 563565.
Gottlieb, Y., Ghanim, M., Chiel, E., Gerling, D., Portnoy, V., Steinberg, S., Tzuri, G., Horowitz, A.R., Belausov, E., Mozes-Daube, N., Kontsedalov, S., Gershon, M., Gal, S., Katzir, N. & Zchori-Fein, E. (2006) Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Applied and Environmental Microbiology 72, 36463652.
Gottlieb, Y., Ghanim, M., Gueguen, G., Kontsedalov, S., Vavre, F., Fleury, F. & Zchori-Fein, E. (2008) Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB Journal 22, 25912599.
Gottlieb, Y., Zchori-Fein, E., Mozes-Daube, N., Kontsedalov, S., Skaljac, M., Brumin, M., Sobol, I., Czosnek, H., Vavre, F., Fleury, F. & Ghanim, M. (2010) The transmission efficiency of Tomato Yellow Leaf Curl Virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. Journal of Virology 84, 93109317.
Gueguen, G., Vavre, F., Gnankine, O., Peterschmitt, M., Charif, D., Chiel, E., Gottlieb, Y., Ghanim, M., Zchori-Fein, E. & Fleury, F. (2010) Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Molecular Ecology 19, 43654376.
Himler, A.G., Adachi-Hagimori, T., Bergen, J.E., Kozuch, A., Kelly, S.E., Tabashnik, B.E., Chiel, E., Duckworth, V.E., Dennehy, T.J., Zchori-Fein, E. & Hunter, M.S. (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332, 254256.
Hu, J., De Barro, P., Zhao, H., Wang, J., Nardi, F. & Liu, S.S. (2011) An extensive field survey combined with a phylogenetic analysis reveals rapid and widespread invasion of two alien whiteflies in China. PLoS ONE 6(1), e16061 (doi:10.1371/journal.pone.0016061).
Ijichi, N., Kondo, N., Matsumoto, R., Shimada, M., Ishikawa, H. & Fukatsu, T. (2002) Internal spatiotemporal population dynamics of infection with three Wolbachia strains in the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae). Applied and Environmental Microbiology 68, 40744080.
Jones, D.R. (2003) Plant viruses transmitted by whiteflies. European Journal of Plant Pathology 109, 195219.
Kontsedalov, S., Zchori-Fein, E., Chiel, E., Gottlieb, Y., Inbar, M. & Ghanim, M. (2008) The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Management Science 64, 789792.
Li, Z.X., Lin, H.Z. & Guo, X.P. (2007) Prevalence of Wolbachia infection in Bemisia tabaci. Current Microbiology 54, 467471.
Miller, W.I., Pabbaraju, K. & Sanderson, K.E. (2000), Fragmentation of 23S rRNA in strains of Proteus and Providencia results from intervening sequences in the rm (rRNA) genes. Journal of Bacteriology 182, 11091117.
Min, K.T. & Benzer, S. (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proceeding of the National Academy of Science USA 94, 1079210796.
Mitsuhashi, W., Saiki, T., Wei, W., Kawakita, H. & Sato, M. (2002) Two novel strains of Wolbachia coexisting in both species of mulberry leafhoppers. Insect Molecular Biology 11, 577584.
Moran, N. & Baumann, P. (1994) Phylogenetics of cytoplasmically inherited microorganisms of arthropods. Trends in Ecology & Evolution 9, 1520.
Moran, N.A., McCutcheon, J.P. & Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics 42, 165190.
Nguyen, R. & Hamon, A.B. (1990) Ash Whitefly, Siphoninus phillyreae (Haliday) (Insecta: Aleyrodidae: Aleyrodinae). Entomology Circular No. 337. Tallahassee, FL, USA, Florida Department of Agriculture and Consumer Services, Division of Plant Industry. Available online at (accessed 18 May 2012).
Nirgianaki, A., Banks, G.K., Frohlich, D.R., Veneti, Z., Braig, H.R., Miller, T.A., Bedford, I.D., Markham, P.G., Savakis, C. & Bourtzis, K. (2003) Wolbachia infections of the whitefly Bemisia tabaci. Current Microbiology 47, 93101.
Oliver, K.M., Russell, J.A., Moran, N.A. & Hunter, M.S. (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Science of the United States of America 100, 18031807.
Perring, T.M. (2001) The Bemisia tabaci species complex. Crop Protection 20, 725737.
Russell, J.A. & Moran, N.A. (2005) Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host. Appled and Environmental Microbiology 71(12), 79877994.
Secker, A.E., Bedford, I.A., Markham, P.G. & William, M.E.C. (1998) Squash, a reliable field indicator for the presence of B biotype of tobacco whitefly, Bemisia tabaci. pp. 837842 in Brighton Crop Protection Conference-Pests and Diseases Farnham, UK, British Crop Protection Council.
Skaljac, M., Zanic, K., Goreta Ban, S., Kontsedalov, S. & Ghanim, M. (2010) Co-infection and localization of secondary symbionts in two whitefly species. BMC Microbiology 10, 142.
Szklarzewicz, T. & Moskal, A. (2001) Ultrastructure, distribution, and transmission of endosymbionts in the whitefly Aleurochiton aceris Modeer (Insecta, Hemiptera, Aleyrodinea). Protoplasma 218, 4553.
Thao, M.L. & Baumann, P. (2004a) Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Applied and Environmental Microbiology 70, 34013406.
Thao, M.L. & Baumann, P. (2004b) Evidence for multiple acquisition of Arsenophonus by whitefly species (Sternorrhyncha: Aleyrodidae). Current Microbiology 48, 140144.
Zanic, K., Cenis, J.L., Kacic, S. & Katalinic, M. (2005) Current Status of Bemisia tabaci in coastal Croatia. Phytoparasitica 33, 6064.
Zchori-Fein, E. & Brown, J.K. (2002) Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Annals of the Entomological Society of America 95, 711718.
Zchori-Fein, E. & Perlman, J.P. (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Molecular Ecology 13, 20092016.
Weeks, A.R. & Breeuwer, J.A.J. (2003) A new bacterium from the Cytophaga-Flavobacterium-Bacteroides phylum that causes sex ratio distortion. pp. 165176in Bourtzis, K. & Miller, T. (Eds) Insect Symbiosis II. Boca Raton, FL, USA, CRC Press.
Werren, J.H., Skinner, S.W. & Huger, A.M. (1986) Male-killing bacteria in a parasitic wasp. Science 231, 990992.


Related content

Powered by UNSILO

Diversity and localization of bacterial symbionts in three whitefly species (Hemiptera: Aleyrodidae) from the east coast of the Adriatic Sea

  • M. Škaljac (a1), K. Žanić (a1), S. Hrnčić (a2), S. Radonjić (a2), T. Perović (a3) and M. Ghanim (a4)...


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.