Skip to main content
SpringerLink
Log in

Prevalence of Endosymbionts in Bemisia tabaci Populations and Their In Vivo Sensitivity to Antibiotics

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Bemisia tabaci can harbor both primary and secondary endosymbionts, and the specific endosymbionts can differ among different B. tabaci biotypes. This study determined (1) the prevalence of the primary endosymbiont Portiera aleyrodidarum and secondary endosymbionts Arsenophonus and Wolbachia in two invasive biotypes (B and Q) and one indigenous biotype (Cv) in China and (2) the in vivo effect of three antibiotics (tetracycline, ampicillin trihydrate, and rifampicin) against the endosymbionts; if an antibiotic substantially inhibits an endosymbiont, it could be used to determine the effect of that endosymbiont on B. tabaci. P. aleyrodidarum and Wolbachia were detected in all the three biotypes, while Arsenophonus was found only in the Q and Cv biotypes. P. aleyrodidarum was found in all tested individuals of the three biotypes. Infection rates of Wolbachia in the B, Cv, and Q biotypes were 58, 68, and 48%, respectively. The infection rate of Arsenophonus was 44% in the Q biotype but only 22% in the Cv biotype. The antibiotics failed to eliminate P. aleyrodidarum from any individual of the B, Cv, and Q biotypes but eliminated the secondary endosymbionts, Arsenophonus and Wolbachia, from 50 to 80% of the adult B. tabaci. The effect of the antibiotics depended on the species of endosymbiont, the antibiotic, the B. tabaci biotype, and various interactions between these factors. When used against Arsenophonus, the efficiency of rifampicin was better than ampicillin and tetracycline, regardless of B. tabaci biotype. When inactivating Wolbachia in Cv and Q biotypes, the efficiency tetracycline was better than ampicillin and rifampicin, and while the efficiency of tetracycline was better than rifampicin and ampicillin when they were used against Wolbachia in B biotype.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Ahmed MZ, Jin GH, Shen Y, Ren SX, Du YZ, Qiu BL (2009) Population and host plant differentiation of the sweetpotato whitefly, Bemisia tabaci (Homoptera: Aleyrodidae), in East, South and Southwest China. Acta Entomol Sin 52:1132–1138

    Google Scholar 

  2. Ahmed MZ, Maruthi MN, Ren SX, Mandour NS, Naveed M, Qiu BL (2009) Genetic variations of Bemisia tabaci populations in cotton growing area from Pakistan, Egypt and China. J Pest Sci. Doi: 10.1007/s10340-009-0279-4

  3. Ahmed MZ, Shatters RG, Ren SX, Jin GH, Mandour NS, Qiu BL (2009) Genetic distinctions among the Mediterranean and Chinese populations of Bemisia tabaci Q biotype and their Wolbachia infection. J Appl Entomol 133:733–741

    Article  CAS  Google Scholar 

  4. Brown JK, Frohlich DR, Rosell RC (1995) The sweetpotato or silverleaf whiteflies: biotypes of Bemisia tabaci or a species complex? Ann Rev Entomol 40:511–534

    Article  CAS  Google Scholar 

  5. Bedford ID, Briddon R, Brown JK, Rosell RC, Markham PG (1994) Geminivirus-transmission and biological characterisation of Bemisia tabaci (Gennadius) biotypes from different geographic regions. Ann Appl Biol 125:311–325

    Article  Google Scholar 

  6. Costa HS, Brown JK (1991) Variation in biological characteristics and in esterase patterns among populations of Bemisia tabaci (Genn) and the association of one population with silverleaf symptom development. Entomol Exp Appl 61:211–219

    Article  Google Scholar 

  7. De Barro PJ, Driver F, Trueman JWH, Curran J (2000) Phylogenetic relationships of world populations of Bemisia tabaci (Gennadius) using ribosomal ITS1. Mol Phylogenet Evol 16:29–36

    Article  PubMed  CAS  Google Scholar 

  8. Perring TM (2001) The Bemisia tabaci species complex. Crop Protect 20:725–737

    Article  Google Scholar 

  9. Bird J, Maramorosch K (1978) Viruses and virus diseases associated with whiteflies. Adv Virus Res 71:233–260

    Google Scholar 

  10. Costa AS, Russell LM (1975) Failure of Bemisia tabaci to breed on cassava plants in Brazil (Homoptera: Aleyroideae). Cienc Cult 27:390–399

    Google Scholar 

  11. Chu D, Zhang YJ, Brown JK, Cong B, Xu BY, Wu QJ, Zhu GR (2006) The introduction of the exotic Q biotype of Bemisia tabaci from the Mediterranean region into China on ornamental crops. Fla Entomol 89:168–174

    Article  Google Scholar 

  12. De Barro PJ, Trueman JWH, Frohlich DR (2005) Bemisia argentifolii is a race of B. tabaci (Hemiptera: Aleyrodidae): the molecular genetic differentiation of B. tabaci populations around the world. Bull Entomol Res 95:193–203

    Article  PubMed  Google Scholar 

  13. De Barro PJ, Driver F (1997) Use of RAPD PCR to distinguish the B biotype from other biotypes of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Aus J Entomol 36:149–152

    Article  Google Scholar 

  14. Brown JK, Coats SA, Bedford ID, Markham PG, Bird J, Frohlich DR (1995) Characterization and distribution of esterase electromorphs in the whitefly, Bemisia tabaci (Genn) (Homoptera: Aleyrodidae). Biochem Genet 33:205–214

    Article  PubMed  CAS  Google Scholar 

  15. Qiu BL, Chen Y, Liu L, Peng W, Ahmed MZ, Du YZ, Ren SX (2009) The identification of three Bemisia tabaci biotypes in China based on their morphological and DNA polymorphism. Prog Nat Sci 19:713–718

    Article  CAS  Google Scholar 

  16. Qiu BL, Ren SX, Wen SY, Mandour NS (2006) Population differentiation of three biotypes of Bemisia tabaci in China by DNA polymorphism. J South China Agric Univ 27:29–34

    CAS  Google Scholar 

  17. Qiu BL, Ren SX, Wen SY, Mandour NS (2003) Biotype identification of the populations of Bemisia tabaci (Homoptera: Aleyrodidae) in China using RAPD-PCR. Acta Entomol Sin 46:605–608

    CAS  Google Scholar 

  18. Qiu BL, Coats SA, Ren SX, Dris AM, Xu CX, Brown JK (2007) Phylogenetic relationships of native and introduced Bemisia tabaci (Homoptera: Aleyrodidae) from China and India based on mtCOI DNA sequencing and host plant comparisons. Prog Nat Sci 17:645–654

    Article  CAS  Google Scholar 

  19. Chu D, Zhang YJ, Cong B, BY Xu, Wu QJ (2005) Identification for Yunnan Q-biotype Bemisia tabaci population. Ch Bull Entomol 42:54–56

    CAS  Google Scholar 

  20. Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Wiley, New York, pp 332–338

    Google Scholar 

  21. Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev Camb Philos Soc 64:409–434

    Article  PubMed  CAS  Google Scholar 

  22. Baumann P, Moran NA, Baumann L (2000) Bacteriocyte-associated endosymbionts of insects. In: Dworkin M (ed) The prokaryotes. Springer, New York

    Google Scholar 

  23. Moran NA, Plague GR, Sandstrom JP, Wilcox JL (2003) A genomic perspective on nutrient provisioning by bacterial symbionts of insects. Proc Natl Acad Sci USA 100:14543–14548

    Article  PubMed  CAS  Google Scholar 

  24. Thao ML, Baumann P (2004) Evidence for multiple acquisition of Arsenophonus by whitefly species (Sternorrhyncha: Aleyrodidae). Curr Microbiol 48:140–144

    Article  PubMed  CAS  Google Scholar 

  25. Clark MA, Baumann L, Munson MA, Baumann P, Campbell BC et al (1992) The eubacterial endosymbionts of whiteflies (Homoptera: Aleyrodidae) constitute a lineage distinct from the endosymbionts of aphids and mealybugs. Curr Microbiol 25:119–123

    Article  Google Scholar 

  26. Everett KDE, Thao M, Horn M, Dyszynski GE, Baumann P (2005) Novel chlamydiae in whiteflies and scale insects:endosymbionts ‘Candidatus Fritschea bemisiae’ strain Falk and ‘Candidatus Fritschea eriococci’ strain Elm. Int J Syst Evol Microbiol 55:1581–1587

    Article  PubMed  CAS  Google Scholar 

  27. Nirgianaki A, Banks GK, Frohlich DR, Veneti Z, Braig HR et al (2003) Wolbachia infections of the whitefly Bemisia tabaci. Curr Microbiol 47:93–101

    Article  PubMed  CAS  Google Scholar 

  28. Thao ML, Baumann L, Hess JM, Falk BW, Ng JC et al (2003) Phylogenetic evidence for two new insect-associated Chlamydia of the family Simkaniaceae. Curr Microbiol 47:46–50

    Article  PubMed  CAS  Google Scholar 

  29. Weeks AR, Velten R, Stouthamer R (2003) Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc R Soc Lond B 270:1857–1865

    Article  Google Scholar 

  30. Costa HS, Westcot DM, Ullman DE, Rosell R, Brown JK, Johnson MW (1995) Morphological variation in Bemisia endosymbionts. Protoplasma 189:194–202

    Article  Google Scholar 

  31. Zchori-Fein E, Brown JK (2002) Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera:Aleyrodidae). Ann Entomol Soc Am 95:711–718

    Article  Google Scholar 

  32. Chiel E, Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Katzir N, Inbar M, Ghanim M (2007) Biotype-dependent secondary symbionts communities in sympatric populations of Bemisia tabaci. Bull Entomol Res 97:407–413

    Article  PubMed  CAS  Google Scholar 

  33. Ruan YM, Xu J, Liu SS (2006) Effects of antibiotics on fitness of the B biotype and a non-B biotype of the whitefly Bemisia tabaci. Entomol Exp Appl 121:159–166

    Article  Google Scholar 

  34. Ruan YM, Liu SS (2005) Detection and phylogenetic analysis of prokaryotic endosymbionts in Bemisia tabaci. Acta Entomol Sin 48:859–865

    CAS  Google Scholar 

  35. Oliver KM, Moran NA, Hunter MS (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102:12795–12800

    Article  PubMed  CAS  Google Scholar 

  36. Oliver K, Russell J, Moran N, Hunter M (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100:1803–1807

    Article  PubMed  CAS  Google Scholar 

  37. Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195

    Article  Google Scholar 

  38. Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989

    Article  PubMed  CAS  Google Scholar 

  39. Costa HS, Toscano NC, Henneberry TJ (1996) Mycetocyte inclusion in the oocytes of Bemisia argentifolii (Homoptera: Aleyrodidae). Ann Entomol Soc Am 89:694–699

    Google Scholar 

  40. Costa HS, Johnson MW, Ullmann DE, Tabashnik BE (1993) The antibiotic, oxytetracycline interferes with Bemisia tabaci oviposition, development, and ability to induce squash silverleaf. Ann Entomol Soc Am 86:740–748

    CAS  Google Scholar 

  41. Costa HS, Westcot DM, Ullman DE, Johnson MW (1993) Ultrastructure of the endosymbionts of the whitefly, Bemisia tabaci and Trialeurodes vaporariorum. Protoplasma 176:106–115

    Article  Google Scholar 

  42. Szklarzewicz T, Agnieszka M (2001) Ultrastructure, distribution, and transmission of endosymbionts in the whitefly Aleurochiton aceris Modeer (Insecta, Hemiptera, Aleyrodinea). Protoplasma 218:45–53

    Article  PubMed  CAS  Google Scholar 

  43. Wilkinson TL (1998) The elimination of intracellular microorganisms from insects: an analysis of antibiotic-treatment in the pea aphid (Acyrthosiphon pisum). Comp Biochem Physiol A 119:871–881

    Article  Google Scholar 

  44. Costa HS, Henneberry TJ, Toscano NC (1997) Effects of antibacterial materials on Bemisia argentifolii (Homoptera: Aleyrodidae) oviposition, growth, survival, and sex ratio. J Eco Entomol 90:333–339

    CAS  Google Scholar 

  45. Mitsuhashi J, Koyama K (1971) Rearing of planthoppers on a holidic diet. Entomol Exp App 14:93–98

    Google Scholar 

  46. Li ZX, Lin HZ, Guo XP (2007) Prevalence of Wolbachia Infection in Bemisia tabaci. Curr Microbiol 54:467–471

    Article  PubMed  CAS  Google Scholar 

  47. Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, Tzuri G, Horowitz AR, 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). App Environ Microbiol 72:3646–3652

    Article  CAS  Google Scholar 

  48. Campbell EA, Korzheva N, Mustaev A, Murakami K, Nair S et al (2001) Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104:901–912

    Article  PubMed  CAS  Google Scholar 

  49. Rajan TV (2004) Relationship of anti microbial activity of tetracyclines to their ability to block the L3 to L4 molt of the human filarial parasite Brugia malayi. Am J Trop Med Hyg 71:24–28

    PubMed  CAS  Google Scholar 

  50. Zhou W, Rousset F, O’Neill S (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc R Soc Lond B 265:509–515

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Einat Zchori-Fein (Agricultural Research Organization, Israel) and the anonymous reviewers for their constructive comments. We also thank Cai-Xia Xu and Xing-Ming Wang (South China Agricultural University, Guangzhou, China) for their technical help in experiments. This research was supported by the National Basic Research Program of China (973 Project, 2009CB119203), the National Department Public Benefit Research Foundation (nyhyzx200803005), and the China National Natural Science Foundation (30671372, 30871678).

Author information

Authors and Affiliations

  1. Department of Entomology, South China Agricultural University, Guangzhou, 510640, People’s Republic of China

    Muhammad Z. Ahmed, Shun-xiang Ren, Xia Xue, Xiao-Xi Li, Gui-hua Jin & Bao-Li Qiu

Authors
  1. Muhammad Z. Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shun-xiang Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xia Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiao-Xi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gui-hua Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bao-Li Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bao-Li Qiu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ahmed, M.Z., Ren, Sx., Xue, X. et al. Prevalence of Endosymbionts in Bemisia tabaci Populations and Their In Vivo Sensitivity to Antibiotics. Curr Microbiol 61, 322–328 (2010). https://doi.org/10.1007/s00284-010-9614-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-010-9614-5

Keywords

Search

Navigation