Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Pantoea Bacteria Isolated from Three Thrips (Frankliniella occidentalis, Frankliniella intonsa, and Thrips tabaci) in Korea and Their Symbiotic Roles in Host Insect Development

  • Gahyeon Jin (Department of Plant Medicals, Andong National University) ;
  • Yonggyun Kim (Department of Plant Medicals, Andong National University)
  • Received : 2023.01.12
  • Accepted : 2023.02.23
  • Published : 2023.06.28
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Abstract

Gut symbionts play crucial roles in host development by producing nutrients and defending against pathogens. Phloem-feeding insects in particular lack essential nutrients in their diets, and thus, gut symbionts are required for their development. Gram-negative Pantoea spp. are known to be symbiotic to the western flower thrips (Frankliniella occidentalis). However, their bacterial characteristics have not been thoroughly investigated. In this study, we isolated three different bacteria (BFoK1, BFiK1, and BTtK1) from F. occidentalis, F. intonsa, and T. tabaci. The bacterial isolates of all three species contained Pantoea spp. Their 16S rRNA sequences indicated that BFoK1 and BTtK1 were similar to P. agglomerans, while BFiK1 was similar to P. dispersa. These predictions were supported by the biochemical characteristics assessed by fatty acid composition and organic carbon utilization. In the bacterial morphological analysis, BFoK1 and BTtK1 were distinct from BFiK1. All these bacteria were relatively resistant to tetracycline compared to ampicillin and kanamycin, in which BFoK1 and BTtK1 were different from BFiK1. Feeding ampicillin (100,000 ppm) reduced the bacterial density in thrips and retarded the development of F. occidentalis. The addition of BFoK1 bacteria, however, rescued the retarded development. These findings indicate that Pantoea bacteria are symbionts to different species of thrips.

Keywords

Acknowledgement

We appreciate Dr. Miltan Roy's technical support of the bacterial isolation from thrips. This work was carried out with the support of the Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ01578901) funded by the Rural Development Administration, Republic of Korea.

References

  1. Ferrari J, Vavre F. 2011. Bacterial symbionts in insects or the story of communities affecting communities. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366: 1389-1400. https://doi.org/10.1098/rstb.2010.0226
  2. Akman Gunduz E, Douglas AE. 2009. Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc. Biol. Sci. 276: 987-991. https://doi.org/10.1098/rspb.2008.1476
  3. Koga R, Meng XY, Tsuchida T, Fukatsu T. 2012. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. Proc. Natl. Acad. Sci. USA 109: E1230-E1237. https://doi.org/10.1073/pnas.1119212109
  4. Andongma AA, Whitten MMA, Sol RD, Hitchings M, Dyson PJ. 2022. Bacterial competition influences the ability of symbiotic bacteria to colonize western flower thrips. Front. Microbiol. 13: 883891.
  5. Salcedo-Porras N, Umana-Diaz C, Bitencourt ROB, Lowenberger C. 2020. The role of bacterial symbionts in triatomines: an evolutionary perspective. Microorganisms 8: 1438.
  6. Beard CB, Dotson EM, Pennington PM, Eichler S, Cordon-Rosales C, Durvasula RV. 2001. Bacterial symbiosis and paratransgenic control of vector-borne Chagas disease. Int. J. Parasitol. 31: 621-627. https://doi.org/10.1016/S0020-7519(01)00165-5
  7. Reitz SR, Gao Y, Kirk WDJ, Hoddle MS, Leiss KA, Funderburk JE. 2020. Invasion biology, ecology, and management of western flower thrips. Annu. Rev. Entomol. 65: 17-37. https://doi.org/10.1146/annurev-ento-011019-024947
  8. He Z, Guo JF, Reitz SR, Lei ZR, Wu SY. 2020. A global invasion by the thrips, Frankliniella occidentalis: Current virus vector status and its management. Insect Sci. 27: 626-645. https://doi.org/10.1111/1744-7917.12721
  9. Rotenberg D, Jacobson AL, Schneweis DJ, Whitfield AE. 2015. Thrips transmission of tospoviruses. Curr. Opin. Virol. 15: 80-89. https://doi.org/10.1016/j.coviro.2015.08.003
  10. de Vries EJ, Jacobs G, Breeuwer JAJ, Mollema C. 2001a. The association of F. occidentalis, Frankliniella occidentalis, with Erwinia species gut bacteria: transient or permanent? J. Invertebr. Pathol. 77: 120-128. https://doi.org/10.1006/jipa.2001.5009
  11. Chanbusarakum L Ullman D. 2008. Characterization of bacterial symbionts in Frankliniella occidentalis (Pergande), Western flower thrips. J. Invertebr. Pathol. 99: 318-325. https://doi.org/10.1016/j.jip.2008.09.001
  12. Facey PD, Meric G, Hitchings MD, Pachebat JA, Hegarty MJ, Chen X, et al. 2015. Draft genomes, phylogenetic reconstruction, and comparative genomics of two novel cohabiting bacterial symbionts isolated from Frankliniella occidentalis. Genome Biol. Evol. 7: 2188-2202. https://doi.org/10.1093/gbe/evv136
  13. de Vries EJ, Jacobs G, Breeuwer JAJ. 2001b. Transmission and growth of gut bacteria in the F. occidentalis, Frankliniella occidentalis. J. Invertebr. Pathol. 77: 129-136. https://doi.org/10.1006/jipa.2001.5010
  14. Woo KS, Ahn SB, Lee SH, Kwon HM. 1994. First record of Frankliniella occidentalis and its distribution and host plants in Korea. Korean J. Appl. Entomol. 33: 127.
  15. Rugman-Jones PF, Hoddle MS, Stouthamer R. 2010. Nuclear mitochondrial barcoding exposes the global pest western flower thrips (Thysanoptera: Thripidae) as two sympatric cryptic species in its native California. Mol. Entomol. 103: 877-886. https://doi.org/10.1603/EC09300
  16. Kim CY, Choi DY, Kang JH, Ahmed S, Kil EJ, Kwon GM, et al. 2021. Thrips infesting hot pepper cultured in greenhouses and variation in gene sequences encoded in TSWV. Korean J. Appl. Entomol. 60: 381-401.
  17. Kim C, Choi D, Lee D, Khan F, Kwon G, Ham E, et al. 2022. Yearly occurrence of thrips infesting hot pepper in greenhouses and differential damages of dominant thrips. Korean J. Appl. Entomol. 61: 319-330
  18. Tailliez P, Pages S, Ginibre N, Boemare N. 2006. New insight into diversity in the genus Xenorhabdus, including the description of ten novel species. Int. J. Syst. Evol. Microbiol. 56: 2805-2818. https://doi.org/10.1099/ijs.0.64287-0
  19. Schaad NW, Jones JB, Chun W. 2000. Laboratory guide for identification of plant pathogenic bacteria. 3rd Edition. American Phytopathological Society Press, St. Paul, MN, USA.
  20. Whitman WB. 2015. Bergey's manual of systematic of archaea and bacteria. John Wiley & Sons, Inc., Hoboken, NJ, USA.
  21. SAS Institute Inc. 1989. SAS/STAT user's guide. SAS Institute, Inc., Cary, NC.
  22. Walterson AM, Stavrinides J. 2015. Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiol. Rev. 39: 968-984. https://doi.org/10.1093/femsre/fuv027
  23. Kim J, Choi O, Kim TS. 2012. An outbreak of onion center rot caused by Pantoea ananatis in Korea. Plant Dis. 96: 1576.
  24. Gitaitis RD, Walcott RR, Wells ML, Perez JCD, Sanders FH. 2003. Transmission of Pantoea ananatis, the causal agent of center rot of onion, by tobacco thrips, Frankliniella fusca. Plant Dis. 87: 675-678. https://doi.org/10.1094/PDIS.2003.87.6.675
  25. Chang, CP, Sung IH, Huang CJ. 2018. Pantoea dispersa causing bulb decay of onion in Taiwan. Australas. Plant Pathol. 47: 609-613. https://doi.org/10.1007/s13313-018-0596-2
  26. Toh WK, Loh PC, Wong HL. 2019. First report of leaf blight of rice caused by Pantoea ananatis and Pantoea dispersa in Malaysia. Plant Dis. 103: 1764.
  27. Ullman DE, Westcot DM, Hunter WB, Mau RFL. 1989. Internal anatomy and morphology of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) with special reference to interactions between thrips and tomato spotted wilt virus. Int. J. Insect Morph. Embryol. 18: 289-310. https://doi.org/10.1016/0020-7322(89)90011-1
  28. de Vries EJ, Jacobs G, Sabelis MW, Menken SBJ, Breeuwer JAJ. 2004. Diet-dependent effects of gut bacteria on their insect host: the symbiosis of Erwinia sp. and western flower thrips. Proc. R. Soc. Lond. Ser. B. Biol. Sci. 271: 2171-2178. https://doi.org/10.1098/rspb.2004.2817
  29. Khan F, Roy MC, Kim Y. 2022. Thelytokous reproduction of onion thrips, Thrips tabaci Lindeman 1889, infesting welsh onion and genetic variation among their subpopulations. Insects 13: 78.
  30. de Vries EJ, van der Wurff AW, Jacobs G, Breeuwer, J.A., 2008. Onion thrips, Thrips tabaci, have gut bacteria that are closely related to the symbionts of the western flower thrips, Frankliniella occidentalis. J. Insect Sci. 8: 1-11. https://doi.org/10.1673/031.008.2301
  31. Dutta B, Barman AK, Srinivasan R, Avci U, Ullman DE, Langston DB, et al. 2014. Transmission of Pantoea ananatis and P. agglomerans, causal agents of center rot of onion (Allium cepa), by onion thrips (Thrips tabaci) through feces. Phytopathology 104: 812-819. https://doi.org/10.1094/PHYTO-07-13-0199-R
  32. Chanbusarakum LJ, Ullman DE. 2009. Distribution and ecology of Frankliniella occidentalis (Thysanoptera: Thripidae) bacterial symbionts. Environ. Entomol. 38: 1069-1077. https://doi.org/10.1603/022.038.0414
  33. Dillon RJ, Vennard CT, Charnley AK. 2000. Exploitation of gut bacteria in the locust. Nature 403: 851.
  34. Wang S, Ghosh AK, Bongio N, Stebbings KA, Lampe DJ, Jacobs-Lorena M. 2012. Fighting malaria with engineered symbiotic bacteria from vector mosquitoes. Proc. Natl. Acad. Sci. USA 109: 12734-12739. https://doi.org/10.1073/pnas.1204158109