Skip to main content

Advertisement

Log in

Population Dynamics of Wolbachia in Laodelphax striatellus (Fallén) Under Successive Stress of Antibiotics

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Wolbachia are the most common symbionts in arthropods; antibiotic treatment for eliminating the symbionts from their host is necessary to investigate the functions. Tetracycline antibiotics are widely used to remove endosymbiont Wolbachia from insect hosts. However, very little has been known on the effects of tetracycline on population size of Wolbachia in small brown planthopper (SBPH), Laodelphax striatellus (Fallén), an important insect pest of rice in Asia. Here, we investigated the dynamics of Wolbachia population density in females and males of L. striatellus by real-time fluorescent quantitative PCR method. The Wolbachia density in females and males of L. striatellus all declined sharply after treatment with 2 mg/mL tetracycline for one generation, and continued to decrease to a level which could not be detected by both qPCR and diagnostic PCR after treated for another generation, then maintained at 0 in the following three generations with continuous antibiotic treatment. Wolbachia infection did not recover in L. striatellus after stopping tetracycline treatment for ten generations. This is the first report to precisely monitor the population dynamics of Wolbachia in L. striatellus during successive tetracycline treatment and after that. The results provide a useful method for evaluating the efficiency of artificial operation of endosymbionts.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Jeyaprakash A, Hoy MA (2000) Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty—three arthropod species. Insect Mol Biol 9:393–405

    Article  CAS  PubMed  Google Scholar 

  2. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia?—a statistical analysis of current data. FEMS Microbiol Lett 281:215–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ (2015) The incidence of bacterial endosymbionts in terrestrial arthropods. Proc R Soc B 282:20150249

    Article  PubMed  Google Scholar 

  4. Teixeira L, Ferreira Á, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Bio 6:e1000002

    Article  CAS  Google Scholar 

  5. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702

    Article  CAS  PubMed  Google Scholar 

  6. Vasanthakrishnan RB, Vanika G, Siva-Jothy JA, Monteith KM, Brown SP, Vale PF (2016) Wolbachia confers sex-specific resistance and tolerance to enteric but not systemic bacterial infection in Drosophila. BioRxiv. https://doi.org/10.1101/045757

    Article  Google Scholar 

  7. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, Hedges M, Rocha BC, Hall-Mendelin S, Day A, Riegler M, Hugo LE, Johnson KN, Kay BH, McGraw EA, Hurk AF, Ryan PA, O'Neill SL (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139:1268–1278

    Article  PubMed  Google Scholar 

  8. Bian GW, Xu Y, Lu P, Xie Y, Xi ZY (2010) The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog 6:e1000833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Bian GW, Joshi D, Dong YM, Lu P, Zhou GL, Pan XL, Xu Y, Dimopoulos G, Xi ZY (2013) Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 340:748–751

    Article  CAS  PubMed  Google Scholar 

  10. Berticat C, Rousset F, Raymond M, Berthomieu A, Weill M (2002) High Wolbachia density in insecticide–resistant mosquitoes. Proc Roy Soc B 269:1413–1416

    Article  Google Scholar 

  11. Duron O, Labbé P, Berticat C, Rousset F, Guillot S, Raymond M, Weill M (2006) High Wolbachia density correlates with cost of infection for insecticide resistant Culex pipiens mosquitoes. Evolution 60:303–314

    Article  CAS  PubMed  Google Scholar 

  12. Hoerauf A, Nissen-Pähle K, Schmetz C, Henkle-Dührsen K, Blaxter ML, Büttner DW, Gallin MY, Al-Qaoud KM, Lucius R, Fleischer B (1999) Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J Clin Invest 103:11–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hoerauf A, Volkmann L, Nissen-Paehle K, Schmetz C, Autenrieth I, Büttner DW, Fleischer B (2000) Targeting of Wolbachia endobacteria in Litomosoides sigmodontis: comparison of tetracyclines with chloramphenicol, macrolides and ciprofloxacin. Trop Med Int Health 5:275–279

    Article  CAS  PubMed  Google Scholar 

  14. Wright JD, Wang BT (1980) Observations on Wolbachiae in mosquitoes. J Invertebr Pathol 35:200–208

    Article  Google Scholar 

  15. Trpis M, Perrone JB, Reissig M, Parker KL (1981) Control of cytoplasmic incompatibility in the Aedes scutellaris complex incompatible crosses become compatible by treatment of larvae with heat or antibiotics. J Hered 72:313–317

    Article  Google Scholar 

  16. Graham RI, Grzywacz D, Mushobozi WL, Wilson K (2012) Wolbachia in a major African crop pest increases susceptibility to viral disease rather than protects. Ecol Lett 15:993–1000

    Article  PubMed  Google Scholar 

  17. Sanada-Morimura S, Matsumura M, Noda H (2013) Male Killing caused by a Spiroplasma symbiont in the small brown planthopper, Laodelphax striatellus. J Hered 104:821–829

    Article  PubMed  Google Scholar 

  18. Wolfgang A, Markus R, Dimitrios N, Christian S (2009) Evidence for low-titre infections in insect symbiosis: Wolbachia in the bark beetle Pityogenes chalcographus (Coleoptera, Scolytinae). Environ Microbiol 11:1923–1933

    Article  CAS  PubMed  Google Scholar 

  19. Schneider DI, Garschall KI, Parker AG, Abd-Alla AM, Miller WJ (2013) Global Wolbachia prevalence, titer fluctuations and their potential of causing cytoplasmic incompatibilities in tsetse flies and hybrids of Glossina morsitans subgroup species. J Invertebr Pathol 112:S104–S115

    Article  PubMed  PubMed Central  Google Scholar 

  20. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ, Leong YS, Dong Y, Axford J, Kriesner P, Lloyd AL, Ritchie SA, O’Neill SL, Hoffmann AA (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476:450

    Article  CAS  PubMed  Google Scholar 

  21. Serbus LR, White PM, Silva JP, Rabe A, Teixeira L, Albertson R, Sullivan W (2015) The impact of host diet on Wolbachia titer in Drosophila. PLoS Pathog 11:e1004777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Monnin D, Kremer N, Berny C, Henri H, Dumet A, Voituron Y, Desouhant E, Vavre F (2016) Influence of oxidative homeostasis on bacterial density and cost of infection in Drosophila-Wolbachia symbioses. J Evol Biol 29:1211–1222

    Article  CAS  PubMed  Google Scholar 

  23. Nault LR (1994) Transmission biology, vector specificity and evolution of planthopper-transmitted plant viruses. In: Nault LR (ed) Planthoppers. Springer, Boston, pp 429–448

    Chapter  Google Scholar 

  24. Otuka A, Matsumura M, Sanada-Morimura S, Takeuchi H, Watanabe T, Ohtsu R, Inoue H (2010) The 2008 overseas mass migration of the small brown planthopper, Laodelphax striatellus, and subsequent outbreak of rice stripe disease in western Japan. Appl Entomol Zool 45:259–266

    Article  Google Scholar 

  25. Gao B, Wu J, Huang S, Mu L, Han Z (2007) Insecticide resistance in field populations of Laodelphax striatellus Fallén (Homoptera: Delphacidae) in China and its possible mechanisms. Int J Pest Manag 54:13–19

    Article  CAS  Google Scholar 

  26. Li Y, Liu X, Guo H (2018) Variations in endosymbiont infection between buprofezin-resistant and susceptible strains of Laodelphax striatellus (Fallén). Curr Microbiol 75:709–715

    Article  CAS  PubMed  Google Scholar 

  27. Hoshizaki S, Shimada T (1995) PCR-based detection of Wolbachia, cytoplasmic incompatibility microorganisms, infected in natural populations of Laodelphax striatellus (homoptera: delphacidae) in central japan: has the distribution of Wolbachia spread recently? Insect Mol Biol 4:237–243

    Article  CAS  PubMed  Google Scholar 

  28. Noda H, Koizumi Y, Zhang Q, Deng KJ (2001) Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera. Insect Biochem Molec 31:727–737

    Article  CAS  Google Scholar 

  29. Zhang YL, Guo HF, Yang Q, Li S, Wang LH, Zhang GF, Fang JC (2012) Overexpression of a P450 gene (CYP6CW1) in buprofezin-resistant Laodelphax striatellus (Fallén). Pestic Biochem Phys 104:277–282

    Article  CAS  Google Scholar 

  30. Koch C, Rainey FA, Stackebrandt E (1994) 16S rDNA studies on members of Arthrobacter and Micrococcus: an aid for their future taxonomic restructing. FEMS Microbiol Lett 123:167–171

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  33. Vanbroekhoven K, Ryngaert A, Wattiau P, Mot R, Springael D (2004) Acinetobacter diversity in environmental samples assessed by 16S rRNA gene PCR–DGGE fingerprinting. FEMS Microbiol Ecol 50:37–50

    Article  CAS  PubMed  Google Scholar 

  34. Alonso C, Warnecke F, Amann R, Pernthaler J (2007) High local and global diversity of Flavobacteria in marine plankton. Environ Microbiol 9:1253–1266

    Article  CAS  PubMed  Google Scholar 

  35. Zhu H, Sun SJ, Dang HY (2008) PCR detection of Serratia spp. using primers targeting pfs and luxS genes involved in AI-2-dependent quorum sensing. Curr Microbiol 57:326–330

    Article  CAS  PubMed  Google Scholar 

  36. Nakamura Y, Kawai S, Yukuhiro F, Ito S, Gotoh T, Kisimoto R, Yanase T, Matsumoto Y, Kageyama D, 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. Appl Environ Microb 75:6757–6763

    Article  CAS  Google Scholar 

  37. Zhou LL, Zhang KJ, Song ZW, Hong XX (2010) Relationship of WO phage and Wolbachia infection in Laodelphax striatellus (Fallén) (Hemiptera: Delphacidae). Acta Entomol Sin 53:978–984

    Google Scholar 

  38. Dossi FCA, Silva EP, Cônsoli FL (2014) Population dynamics and growth rates of endosymbionts during Diaphorina citri (Hemiptera, Liviidae) ontogeny. Microb Ecol 68:881–889

    Article  PubMed  Google Scholar 

  39. Whelan JA, Russell NB, Whelan MA (2003) A method for the absolute quantification of cDNA using real-time PCR. J Immunol Methods 278:261–269

    Article  CAS  PubMed  Google Scholar 

  40. Bustin SA, Benes V, Nolan T, Pfaffl MW (2005) Quantitative real-time RT-PCR—a perspective. J Mol Endocrinol 34:597–601

    Article  CAS  PubMed  Google Scholar 

  41. Kubista M, Andrade JM, Bengtsson M, Forootan A, Jonák J, Linda K, Sindelka R, Sjöback R, Sjögreen B, Strömbom L, Ståhlberg A, Zoric N (2006) The real-time polymerase chain reaction. Mol Aspects Med 27:95–125

    Article  CAS  PubMed  Google Scholar 

  42. VanGuilder HD, Vrana KE, Freeman WM (2008) Twenty-five years of quantitative PCR for gene expression analysis. Biotechniques 44:619–626

    Article  CAS  PubMed  Google Scholar 

  43. Garrido-Maestu A, Chapela MJ, Vieites JM, Cabado AG (2015) lolB gene, a valid alternative for qPCR detection of Vibrio cholerae in food and environmental samples. Food Microbiol 46:535–540

    Article  CAS  PubMed  Google Scholar 

  44. Steeples LR, Guiver M, Jones NP (2016) Real-time PCR using the 529 bp repeat element for the diagnosis of atypical ocular toxoplasmosis. Brit J Ophthalmol 100:200–203

    Article  Google Scholar 

  45. Li YY, Floate KD, Fields PG, Pang BP (2014) Review of treatment methods to remove Wolbachia bacteria from arthropods. Symbiosis 62:1–15

    Article  CAS  Google Scholar 

  46. Zhong Y, Li ZX (2013) Influences of tetracycline on the reproduction of the B biotype of Bemisia tabaci (Homoptera: Aleyrodidae). Appl Entomol Zool 48:241–246

    Article  CAS  Google Scholar 

  47. Zha XF, Zhang WJ, Zhou CY, Zhang LY, Xiang ZH, Xia QY (2014) Detection and characterization of Wolbachia infection in silkworm. Genet Mol Biol 37:573–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Pike N, Kingcombe R (2009) Antibiotic treatment leads to the elimination of Wolbachia endosymbionts and sterility in the diplodiploid collembolan Folsomia candida. BMC Biol 7:54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Grenier S, Gomes SM, Pintureau B, Lassablière F, Bolland P (2002) Use of tetracycline in larval diet to study the effect of Wolbachia on host fecundity and clarify taxonomic status of Trichogramma species in cured bisexual lines. J Invertebr Pathol 80:13–21

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Yueliang Zhang at the Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, China, for collecting the small brown planthopper, Laodelphax striatellus.

Funding

This research was supported by grants from the National Natural Science Foundation of China (Grant No. 31672027) and the Independent Innovation Fund of Agricultural Science and Technology in Jiangsu province, China (cx(16)1001).

Author information

Authors and Affiliations

Authors

Contributions

HG conceived the experiments. HG designed the experiments. YL collected the data. HG, YL, and XL analyzed the data. YL and HG wrote and reviewed the manuscript.

Corresponding author

Correspondence to Huifang Guo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Liu, X. & Guo, H. Population Dynamics of Wolbachia in Laodelphax striatellus (Fallén) Under Successive Stress of Antibiotics. Curr Microbiol 76, 1306–1312 (2019). https://doi.org/10.1007/s00284-019-01762-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-019-01762-0

Navigation