Obligate association with gut bacterial symbiont in Japanese populations of the southern green stinkbug Nezara viridula (Heteroptera: Pentatomidae)

  • Akiyo Tada
  • Yoshitomo Kikuchi
  • Takahiro Hosokawa
  • Dmitry L. Musolin
  • Kenji Fujisaki
  • Takema Fukatsu
Original Research Paper

Abstract

The southern green stinkbug Nezara viridula (Linnaeus) has a number of sac-like outgrowths, called crypts, in a posterior section of the midgut, wherein a specific bacterial symbiont is harbored. In previous studies on N. viridula from Hawaiian populations, experimental elimination of the symbiont caused few fitness defects in the host insect. Here we report that N. viridula from Japanese populations consistently harbors the same gammaproteobacterial gut symbiont, but, in contrast with previous work, experimental sterilization of the symbiont resulted in severe nymphal mortality, indicating an obligate host–symbiont relationship. Considering worldwide host–symbiont association and these experimental data, we suggest that N. viridula is generally and obligatorily associated with the gut symbiont, but that the effect of the symbiont on host biology may be different among geographic populations. Possible environmental factors that may affect the host–symbiont relationship are discussed.

Keywords

Nezara viridula Symbiotic bacterium Midgut crypts Gammaproteobacteria Obligate symbiosis 

References

  1. Abe Y, Mishiro K, Takanashi M (1995) Symbiont of brown-winged green bug, Plautia stali Scott. Jpn J Appl Entomol Zool 39:109–115CrossRefGoogle Scholar
  2. Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Interscience, New YorkGoogle Scholar
  3. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Marine Biol Biotechnol 3:294–299PubMedGoogle Scholar
  4. Fukatsu T, Hosokawa T (2002) Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. Appl Environ Microbiol 68:389–396PubMedCrossRefGoogle Scholar
  5. Fukatsu T, Nikoh N (1998) Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Appl Environ Microbiol 64:3599–3606PubMedGoogle Scholar
  6. Glasgow H (1914) The gastric caeca and the caecal bacteria of the Heteroptera. Biol Bull 3:101–171CrossRefGoogle Scholar
  7. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321PubMedCrossRefGoogle Scholar
  8. Hirose E, Panizzi AR, De Souza JT, Cattelan AJ, Aldrich JR (2006) Bacteria in the gut of southern green stink bug (Heteroptera: Pentatomidae). Ann Entomol Soc Am 99:91–95CrossRefGoogle Scholar
  9. 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:e337PubMedCrossRefGoogle Scholar
  10. Kikuchi Y (2009) Endosymbiotic bacteria in insects: their diversity and culturability. Microbes Environ 24:195–204PubMedCrossRefGoogle Scholar
  11. Kikuchi Y, Hosokawa T, Fukatsu T (2007) Insect-microbe mutualism without vertical transmission: a stinkbug acquires beneficial gut symbiont from environment every generation. Appl Environ Microbiol 73:4308–4316PubMedCrossRefGoogle Scholar
  12. Kikuchi Y, Hosokawa T, Nikoh N, Meng XY, Kamagata Y, Fukatsu T (2009) Host–symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biol 7:2PubMedCrossRefGoogle Scholar
  13. Kiritani K (2011) Impacts of global warming on Nezara viridula and its native congeneric species. J Asia Pac Entomol 14:221–226CrossRefGoogle Scholar
  14. Musolin DL (2007) Insects in a warmer world: ecological, physiological and life-history responses of true bugs (Heteroptera) to climate change. Glob Change Biol 13:1565–1585CrossRefGoogle Scholar
  15. Prado SS, Almeida RP (2009) Phylogenetic placement of pentatomid stink bug gut symbionts. Curr Microbiol 58:64–69Google Scholar
  16. Prado SS, Rubinoff D, Almeida RPP (2006) Vertical transmission of a pentatomid caeca-associated symbiont. Ann Entomol Soc Am 99:577–585CrossRefGoogle Scholar
  17. Prado SS, Golden M, Follett PA, Daugherty MP, Almeida RP (2009) Demography of gut symbiotic and aposymbiotic Nezara viridula L. (Hemiptera: Pentatomidae). Environ Entomol 38:103–109PubMedCrossRefGoogle Scholar
  18. R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
  19. Schaefer CW, Panizzi AR (2000) Heteroptera of economic importance. CRC Press, FloridaCrossRefGoogle Scholar
  20. Swofford DL (2001) PAUP* version 4.0b10 [computer program]. Sinauer, SunderlandGoogle Scholar
  21. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  22. Todd JW (1989) Ecology and behavior of Nezara viridula. Annu Rev Entomol 34:273–292CrossRefGoogle Scholar
  23. Tougou D, Musolin DL, Fujisaki K (2009) Some like it hot! Rapid climate change promotes changes in distribution ranges of Nezara viridula and Nezara antennata in Japan. Entomol Exp Appl 130:249–258CrossRefGoogle Scholar
  24. Weirauch C, Schuh RT (2011) Systematics and evolution of Heteroptera: 25 years of progress. Annu Rev Entomol 56:487–510PubMedCrossRefGoogle Scholar
  25. Yukawa J, Kiritani K, Kawasawa T, Higashiura Y, Sawamura N, Nakada K, Gyotoku N, Tanaka A, Kamitani S, Matsuo K, Yamauchi S, Takematsu Y (2009) Northward range expansion by Nezara viridula (Hemiptera: Pentatomidae) in Shikoku and Chugoku Districts, Japan, possibly due to global warming. Appl Entomol Zool 44:429–437CrossRefGoogle Scholar

Copyright information

© The Japanese Society of Applied Entomology and Zoology 2011

Authors and Affiliations

  • Akiyo Tada
    • 1
  • Yoshitomo Kikuchi
    • 2
  • Takahiro Hosokawa
    • 3
  • Dmitry L. Musolin
    • 4
    • 5
  • Kenji Fujisaki
    • 1
  • Takema Fukatsu
    • 3
  1. 1.Graduate School of AgricultureKyoto UniversityKyotoJapan
  2. 2.National Institute of Advanced Industrial Science and Technology (AIST)Hokkaido CenterToyohiraJapan
  3. 3.National Institute of Advanced Industrial Science and Technology (AIST)Tsukuba CenterTsukubaJapan
  4. 4.Department of Forest Protection and Game ManagementSaint Petersburg State Forest Technical AcademySt. PetersburgRussia
  5. 5.Department of EntomologySaint Petersburg State UniversitySaint PetersburgRussia

Personalised recommendations