Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Infection Density Dynamics and Phylogeny of Wolbachia Associated with Coconut Hispine Beetle, Brontispa longissima (Gestro) (Coleoptera: Chrysomelidae), by Multilocus Sequence Type (MLST) Genotyping

  • Ali, Habib (State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University) ;
  • Muhammad, Abrar (State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University) ;
  • Hou, Youming (State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University)
  • Received : 2017.12.08
  • Accepted : 2018.03.03
  • Published : 2018.05.28
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Abstract

The intracellular bacterium Wolbachia pipientis is widespread in arthropods. Recently, possibilities of novel Wolbachia-mediated hosts, their distribution, and natural rate have been anticipated, and the coconut leaf beetle Brontispa longissima (Gestro) (Coleoptera: Chrysomelidae), which has garnered attention as a serious pest of palms, was subjected to this interrogation. By adopting Wolbachia surface protein (wsp) and multilocus sequence type (MLST) genotypic systems, we determined the Wolbachia infection density within host developmental stages, body parts, and tissues, and the results revealed that all the tested samples of B. longissima were infected with the same Wolbachia strain (wLog), suggesting complete vertical transmission. The MLST profile elucidated two new alleles (ftsZ-234 and coxA-266) that define a new sequence type (ST-483), which indicates the particular genotypic association of B. longissima and Wolbachia. The quantitative real-time PCR analysis revealed a higher infection density in the eggs and adult stage, followed by the abdomen and reproductive tissues, respectively. However, no significant differences were observed in the infection density between sexes. Moreover, the wsp and concatenated MLST alignment analysis of this study with other known Wolbachia-mediated arthropods revealed similar clustering with distinct monophyletic supergroup B. This is the first comprehensive report on the prevalence, infection dynamics, and phylogeny of the Wolbachia endosymbiont in B. longissima, which demonstrated that Wolbachia is ubiquitous across all developmental stages and distributed in the entire body of B. longissima. Understanding the Wolbachia infection dynamics would provide useful insight to build a framework for future investigations, understand its impacts on host physiology, and exploit it as a potential biocontrol agent.

Keywords

References

  1. Jolivet P, Santiago-Blay JA, Schmitt M. (eds.). 2008. Research on Chrysomelidae. Brill Leiden, The Netherlands.
  2. Wesseler J, Fall EH. 2010. Potential damage costs of Diabrotica virgifera virgifera infestation in Europe - the 'no control' scenario. J. Appl. Entomol. 134: 385-394. https://doi.org/10.1111/j.1439-0418.2010.01510.x
  3. Staines C. 2012. Catalog of the hispines of the World (Coleoptera: Chrysomelidae: Cassidinae). Tribe Cryptonychini. Online publication available from http://entomology.si.edu/ Collections_Coleoptera-Hispines.html (last accessed January 2014).
  4. Konishi K, Nakamura S, Takasu K. 2007. Invasion of the coconut hispine beetle, Brontispa longissima: current situation and control measures in Asia. Presented at the NIAES International Symposium 2007. Invasive Alien Species in Monsoon Asia: Status and Control. Epochal Tsukuba, Japan, October 22-23, 2007.
  5. Sugeno W, Kawazu K, Takano S, Nakamura S, Mochizuki A. 2011. Suitability of monocots for rearing alien coconut pest Brontispa longissima (Coleoptera: Chrysomelidae). Ann. Entomol. Soc. Am. 104: 682-687. https://doi.org/10.1603/AN10146
  6. Lu Y, Zeng L, Wang L, Zhou R. 2003. Risk analysis of palm leaf beetle Brontispa longissima (Gestro). Entomol. J. East Chin. 13: 17-20.
  7. Zhang X, Tang B, Hou Y. 2015. A rapid diagnostic technique to discriminate between two pests of palms, Brontispa longissima and Octodonta nipae (Coleoptera: Chrysomelidae), for quarantine applications. J. Econ. Entomol. 108: 95-99. https://doi.org/10.1093/jee/tou025
  8. Yamashita A, Takasu K. 2010. Suitability of potential host plants in Japan for immature development of the coconut hispine beetle, Brontispa longissima (Gestro) (Coleoptera: Chrysomelidae). Japan Agric. Res. Q. 44: 143-149. https://doi.org/10.6090/jarq.44.143
  9. Hou Y, Miao Y, Zhang Z. 2014. Study on life parameters of the invasive species Octodonta nipae (Coleoptera: Chrysomelidae) on different palm species, under laboratory conditions. J. Econ. Entomol. 107: 1486-1495. https://doi.org/10.1603/EC14119
  10. Wu Q, Zeng L, Sun J-C, Liang G, Lu Y. 2006. Control efficiency of Metarhizium anisopliae on Brontispal longissima (Gestro) in field. J. Shandong Agric. Univ. 37: 568.
  11. Zhong M, Shen Z-R. 2004. Infection of the endosymbiont Wolbachia in population of Trichogramma evanescens in China. Acta Entomol. Sin. 6: 732-737.
  12. Harris HL, Brennan LJ, Keddie BA, Braig HR. 2010. Bacterial symbionts in insects: balancing life and death. Symbiosis 51: 37-53. https://doi.org/10.1007/s13199-010-0065-3
  13. Mason CJ, Raffa KF. 2014. Acquisition and structuring of midgut bacterial communities in gypsy moth (Lepidoptera: Erebidae) larvae. Environ. Entomol. 43: 595-604. https://doi.org/10.1603/EN14031
  14. Dillon R, Dillon V. 2004. The gut bacteria of insects: nonpathogenic interactions. Annu. Rev. Entomol. 49: 71-92. https://doi.org/10.1146/annurev.ento.49.061802.123416
  15. Douglas AE. 2009. The microbial dimension in insect nutritional ecology. Funct. Ecol. 23: 38-47. https://doi.org/10.1111/j.1365-2435.2008.01442.x
  16. Moya A, Pereto J, Gil R, Latorre A. 2008. Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat. Rev. Genet. 9: 218-229. https://doi.org/10.1038/nrg2319
  17. Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T. 2006. Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol. 4: e337. https://doi.org/10.1371/journal.pbio.0040337
  18. Yen JH, Barr AR. 1973. The etiological agent of cytoplasmic incompatibility in Culex pipiens. J. Invertebr. Pathol. 22: 242-250. https://doi.org/10.1016/0022-2011(73)90141-9
  19. Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ. 2010. Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329: 212-215. https://doi.org/10.1126/science.1188235
  20. Lu F, Kang X, Lorenz G, Espino L, Jiang M, Way MO. 2014. Culture-independent analysis of bacterial communities in the gut of rice water weevil (Coleoptera: Curculionidae). Ann. Entomol. Soc. Am. 107: 592-600. https://doi.org/10.1603/AN13145
  21. Pernice M, Simpson SJ, Ponton F. 2014. Towards an integrated understanding of gut microbiota using insects as model systems. J. Insect Physiol. 69: 12-18. https://doi.org/10.1016/j.jinsphys.2014.05.016
  22. Mouton L, Henri H, Bouletreau M, Vavre F. 2003. Strain- specific regulation of intracellular Wolbachia density in multiply infected insects. Mol. Ecol. 12: 3459-3465. https://doi.org/10.1046/j.1365-294X.2003.02015.x
  23. Koga R, Tsuchida T, Fukatsu T. 2003. Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc. R. Soc. Lond. B 270: 2543-2550. https://doi.org/10.1098/rspb.2003.2537
  24. Hoffmann A, Turelli M. 1997. Cytoplasmic incompatibility in insects, pp. 42-80. In O'Neill SL, Werren JH, Hoffmann AA (eds.). Influential Passengers. Oxford University Press, New York.
  25. Bouchon D, Rigaud T, Juchault P. 1998. Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proc. R. Soc. Lond. B 265: 1081-1090. https://doi.org/10.1098/rspb.1998.0402
  26. Fialho RF, Stevens L. 2000. Male-killing Wolbachia in a flour beetle. Proc. R. Soc. Lond. B 267: 1469-1473. https://doi.org/10.1098/rspb.2000.1166
  27. Pannebakker BA, Pijnacker LP, Zwaan BJ, Beukeboom LW. 2004. Cytology of Wolbachia-induced parthenogenesis in Leptopilina clavipes (Hymenoptera: Figitidae). Genome 47: 299- 303. https://doi.org/10.1139/g03-137
  28. Werren JH. 1997. Biology of Wolbachia. Annu. Rev. Entomol. 42: 587-609. https://doi.org/10.1146/annurev.ento.42.1.587
  29. Jiggins FM, Bentley JK, Majerus ME, Hurst GD. 2001. How many species are infected with Wolbachia? Cryptic sex ratio distorters revealed to be common by intensive sampling. Proc. R. Soc. Lond. B 268: 1123-1126. https://doi.org/10.1098/rspb.2001.1632
  30. Jeyaprakash A, Hoy M. 2000. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty- three arthropod species. Insect Mol. Biol. 9: 393-405. https://doi.org/10.1046/j.1365-2583.2000.00203.x
  31. Werren JH, Windsor DM. 2000. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc. R. Soc. Lond. B 267: 1277-1285. https://doi.org/10.1098/rspb.2000.1139
  32. Werren JH, Windsor D, Guo L. 1995. Distribution of Wolbachia among neotropical arthropods. Proc. R. Soc. Lond. B 262: 197-204. https://doi.org/10.1098/rspb.1995.0196
  33. Oh HW, Kim MG, Shin SW, Bae KS, Ahn YJ, Park HY. 2000. Ultrastructural and molecular identification of a Wolbachia endosymbiont in a spider, Nephila clavata. Insect Mol. Biol. 9: 539-543. https://doi.org/10.1046/j.1365-2583.2000.00218.x
  34. Tsuchida T, Koga R, Fukatsu T. 2004. Host plant specialization governed by facultative symbiont. Science 303: 1989. https://doi.org/10.1126/science.1094611
  35. Bordenstein SR, Paraskevopoulos C, Hotopp JCD, Sapountzis P, Lo N, Bandi C, et al. 2009. Parasitism and mutualism in Wolbachia: what the phylogenomic trees can and cannot say. Mol. Biol. Evol. 26: 231-241.
  36. Salunke BK, Salunkhe RC, Patole MS, Shouche YS. 2010. Wolbachia and termite association: present status and future implications. J. Biosci. 35: 171-175. https://doi.org/10.1007/s12038-010-0020-8
  37. Ali H, Hou Y, Tang B, Shi ZH, Huang B, Muhammad A, et al. 2016. A way of reproductive manipulation and biology of Wolbachia pipientis. J. Exp. Biol. Agric. Sci. 4: 156-168.
  38. Werren JH, Zhang W, Guo LR. 1995. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc. R. Soc. Lond. B 261: 55-63. https://doi.org/10.1098/rspb.1995.0117
  39. Vandekerckhove TT, Watteyne S, Willems A, Swings JG, Mertens J, Gillis M. 1999. Phylogenetic analysis of the 16S rDNA of the cytoplasmic bacterium Wolbachia from the novel host Folsomia candida (Hexapoda, Collembola) and its implications for wolbachial taxonomy. FEMS Microbiol. Lett. 180: 279-286. https://doi.org/10.1111/j.1574-6968.1999.tb08807.x
  40. Rowley SM, Raven RJ, McGraw EA. 2004. Wolbachia pipientis in Australian spiders. Curr. Microbiol. 49: 208-214.
  41. Casiraghi M, Bordenstein S, Baldo L, Lo N, Beninati T, Wernegreen J, et al. 2005. Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. Microbiology 151: 4015-4022. https://doi.org/10.1099/mic.0.28313-0
  42. Lo N, Paraskevopoulos C, Bourtzis K, O'Neill S, Werren J, Bordenstein S, et al. 2007. Taxonomic status of the intracellular bacterium Wolbachia pipientis. Int. J. Syst. Evol. Microbiol. 57: 654-657. https://doi.org/10.1099/ijs.0.64515-0
  43. Baldo L, Hotopp JCD, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR, et al. 2006. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl. Environ. Microbiol. 72: 7098-7110. https://doi.org/10.1128/AEM.00731-06
  44. 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. https://doi.org/10.1098/rspb.1998.0324
  45. Kaakeh W. 2005. Longevity, fecundity, and fertility of the red palm weevil, Rynchophorus ferrugineus Olivier (Coleoptera: Curculionidae) on natural and artificial diets. Emirates J. Agric. Sci. 17: 23-33.
  46. Avtzis DN, Doudoumis V, Bourtzis K. 2014. Wolbachia infections and mitochondrial diversity of two chestnut feeding Cydia species. PLoS One 9: e112795. https://doi.org/10.1371/journal.pone.0112795
  47. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739. https://doi.org/10.1093/molbev/msr121
  48. Hoffmann M, Coy M, Pelz-Stelinski K. 2014. Wolbachia infection density in populations of the Asian citrus psyllid (Hemiptera: Liviidae). Environ. Entomol. 43: 1215-1222. https://doi.org/10.1603/EN14193
  49. Kyei-Poku G, Colwell D, Coghlin P, Benkel B, Floate K. 2005. On the ubiquity and phylogeny of Wolbachia in lice. Mol. Ecol. 14: 285-294.
  50. Lo N, Casiraghi M, Salati E, Bazzocchi C, Bandi C. 2002. How many Wolbachia supergroups exist? Mol. Biol. Evol. 19: 341-346. https://doi.org/10.1093/oxfordjournals.molbev.a004087
  51. Hamm CA, Begun DJ, Vo A, Smith CC, Saelao P, Shaver AO, et al. 2014. Wolbachia do not live by reproductive manipulation alone: infection polymorphism in Drosophila suzukii and D. subpulchrella. Mol. Ecol. 23: 4871-4885. https://doi.org/10.1111/mec.12901
  52. Liu Y, Zhang Y, Jiang Q, Rao M, Sheng Z, Zhang Y, et al. 2015. Identification of valid housekeeping genes for real- time quantitative PCR analysis of collapsed lung tissues of neonatal somatic cell nuclear transfer-derived cattle. Cell. Reprogram. 17: 360-367. https://doi.org/10.1089/cell.2015.0024
  53. Sun W, Jin Y, He L, Lu W-C, Li M. 2010. Suitable reference gene selection for different strains and developmental stages of the carmine spider mite, Tetranychus cinnabarinus, using quantitative real-time PCR. J. Insect Sci. 10: 208.
  54. Song H, Zhang X, Shi C, Wang S, Wu A, Wei C. 2016. Selection and verification of candidate reference genes for mature microRNA expression by quantitative RT-PCR in the tea plant (Camellia sinensis). Genes 7: 25. https://doi.org/10.3390/genes7060025
  55. Bustin SA. 2000. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 25: 169-193. https://doi.org/10.1677/jme.0.0250169
  56. Ming Q-L, Shen J-F, Cheng C, Liu C-M, Feng Z-J. 2015. Wolbachia infection dynamics in Tribolium confusum (Coleoptera: Tenebrionidae) and their effects on host mating behavior and reproduction. J. Econ. Entomol. 108: 1408-1415. https://doi.org/10.1093/jee/tov053
  57. Dossi FCA, da Silva EP, Consoli FL. 2014. Population dynamics and growth rates of endosymbionts during Diaphorina citri (Hemiptera, Liviidae) ontogeny. Microb. Ecol. 68: 881-889. https://doi.org/10.1007/s00248-014-0463-9
  58. Rousset F, Braig HR, O'Neill SL. 1999. A stable triple Wolbachia infection in Drosophila with nearly additive incompatibility effects. Heredity 82: 620-627. https://doi.org/10.1046/j.1365-2540.1999.00501.x
  59. Noda H, Koizumi Y, Zhang Q, Deng K. 2001. Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera. Insect Biochem. Mol. Biol. 31: 727-737. https://doi.org/10.1016/S0965-1748(00)00180-6
  60. Dobson SL, Bourtzis K, Braig HR, Jones BF, Zhou W, Rousset F, et al. 1999. Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem. Mol. Biol. 29: 153-160. https://doi.org/10.1016/S0965-1748(98)00119-2
  61. Kose H, Karr TL. 1995. Organization of Wolbachia pipientis in the Drosophila fertilized egg and embryo revealed by an anti-Wolbachia monoclonal antibody. Mech. Dev. 51: 275-288. https://doi.org/10.1016/0925-4773(95)00372-X
  62. Serbus LR, Sullivan W. 2007. A cellular basis for Wolbachia recruitment to the host germline. PLoS Pathog. 3: e190. https://doi.org/10.1371/journal.ppat.0030190
  63. Kondo N, Shimada M, Fukatsu T. 1999. High prevalence of Wolbachia in the azuki bean beetle Callosobruchus chinensis (Coleoptera, Bruchidae). Zool. Sci. 16: 955-962. https://doi.org/10.2108/zsj.16.955
  64. Cheng Q, Ruel T, Zhou W, Moloo S, Majiwa P, O'Neill S, et al. 2000. Tissue distribution and prevalence of Wolbachia infections in tsetse flies, Glossina spp. Med. Vet. Entomol. 14: 44-50. https://doi.org/10.1046/j.1365-2915.2000.00202.x
  65. Rozek M, Lachowska D, Holecova M, Kajtoch L. 2009. Karyology of parthenogenetic weevils (Coleoptera, Curculionidae): do meiotic prophase stages occur? Micron 40: 881-885. https://doi.org/10.1016/j.micron.2009.06.006
  66. 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. Mol. Ecol. 20: 853-868. https://doi.org/10.1111/j.1365-294X.2010.04980.x
  67. Rasgon JL, Scott TW. 2004. Phylogenetic characterization of Wolbachia symbionts infecting Cimex lectularius L. and Oeciacus vicarius Horvath (Hemiptera: Cimicidae). J. Med. Entomol. 41: 1175-1178. https://doi.org/10.1603/0022-2585-41.6.1175
  68. Lachowska D, Kajtoch Ł, Knutelski S. 2010. Occurrence of Wolbachia in central European weevils: correlations with host systematics, ecology, and biology. Entomol. Exp. Appl. 135: 105-118. https://doi.org/10.1111/j.1570-7458.2010.00974.x
  69. Zabalou S, Riegler M, Theodorakopoulou M, Stauffer C, Savakis C, Bourtzis K. 2004. Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proc. Natl. Acad. Sci. USA 101: 15042-15045. https://doi.org/10.1073/pnas.0403853101
  70. Bourtzis K. 2008. Wolbachia-based technologies for insect pest population control. Adv. Exp. Med. Biol. 627: 104-113.
  71. Calvitti M, Moretti R, Lampazzi E, Bellini R, Dobson SL. 2010. Characterization of a new Aedes albopictus (Diptera: Culicidae)-Wolbachia pipientis (Rickettsiales: Rickettsiaceae) symbiotic association generated by artificial transfer of the wPip strain from Culex pipiens (Diptera: Culicidae). J. Med. Entomol. 47: 179-187.
  72. Walker T, Johnson P, Moreira L, Iturbe-Ormaetxe I, Frentiu F, McMeniman C, et al. 2011. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476: 450-453. https://doi.org/10.1038/nature10355
  73. Hoffmann AA, Ross PA, Rasic G. 2015. Wolbachia strains for disease control: ecological and evolutionary considerations. Evol. Appl. 8: 751-768. https://doi.org/10.1111/eva.12286
  74. Mercot H, Charlat S. 2004. Wolbachia infections in Drosophila melanogaster and D. simulans: polymorphism and levels of cytoplasmic incompatibility. Genetica 120: 51-59. https://doi.org/10.1023/B:GENE.0000017629.31383.8f
  75. Cross HF, Haarbrink M, Egerton G, Yazdanbakhsh M, Taylor MJ. 2001. Severe reactions to filarial chemotherapy and release of Wolbachia endosymbionts into blood. Lancet 358: 1873-1875. https://doi.org/10.1016/S0140-6736(01)06899-4
  76. Saint Andre Av, Blackwell NM, Hall LR, Hoerauf A, Brattig NW, Volkmann L, et al. 2002. The role of endosymbiotic Wolbachia bacteria in the pathogenesis of river blindness. Science 295: 1892-1895. https://doi.org/10.1126/science.1068732

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