Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T16:40:13.741Z Has data issue: false hasContentIssue false
  • English
  • Français

Habitat visualization, acquisition features and necessity of the gammaproteobacterial symbiont of pistachio stink Bug, Acrosternum heegeri (Hem.: Pentatomidae)

Published online by Cambridge University Press:  13 June 2019

M. Kashkouli ,
Y. Fathipour Open the ORCID record for Y. Fathipour [Opens in a new window]  and
M. Mehrabadi
M. Kashkouli
Affiliation:
Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, P.O.Box 14115-336, Tehran, Iran
Y. Fathipour*
Affiliation:
Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, P.O.Box 14115-336, Tehran, Iran
M. Mehrabadi
Affiliation:
Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, P.O.Box 14115-336, Tehran, Iran
*
*Author for correspondence Phone: +98 21 48292301 Fax: +98 21 48292200 E-mail: fathi@modares.ac.ir
Get access Rights & Permissions [Opens in a new window]

Abstract

Plant-sucking stinkbugs are especially associated with mutualistic gut bacterial symbionts. Here, we explored the symbiotic relationship of a pistachio stinkbug, Acrosternum heegeri Fieber by histological, fluorescence in situ hybridization (FISH), real-time PCR and molecular phylogenetic techniques. Furthermore, the effects of the symbiont on the resting/wandering behaviors of the newborn nymphs, pre-adult survival rates, and stage compositions were investigated. Transmission electron microscopy and real-time PCR analyses showed that a rod-shaped gammaproteobacterium was persistently located within the posterior midgut crypts. Molecular phylogenetic and FISH techniques strongly suggested that this symbiont should be placed in the genus Pantoea of the Enterobacteriales. Scanning electron microscopy confirmed the presence of the bacterial cells on the egg surface which the surface sterilization of the eggs resulted in the successful removal of the symbiont from the eggs. Symbiotic and aposymbiotic A. heegeri showed no significant differences in the wandering behaviors of the first nymphal stages, while the symbiont-free insects suffered retarded growth and lower survivability. Together, the results highlight the habitat and acquisition features of Pantoea symbiont and its contribution in A. heegeri biology that might help us for better pest management in the future.

Keywords

Heritable symbiontpentatomidaegammaproteobacteriasymbiont elimination
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 1 , February 2020 , pp. 22 - 33
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akman, L., Yamashita, A., Watanabe, H., Oshima, K., Shiba, T., Hattori, M. & Aksoy, S. (2002) Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nature Genetics 32, 402–407.Google Scholar
Bacchetti De Gregoris, T., Aldred, N., Clare, A.S. & Burgess, J.G. (2011) Improvement of phylum- and class-specific primers for real-time PCR quantification of bacterial taxa. Journal of Microbiological Methods 86, 351–356.Google Scholar
Bagheri, F., Talebi, K. & Hosseininaveh, V. (2010) Cellular energy allocation of pistachio green stink bug, Brachynema germari Kol. (Hemiptera: Pentatomidae) in relation to juvenoid pyriproxyfen. African Journal of Biotechnology 9, 5746–5753.Google Scholar
Bansal, R., Michel, A.P. & Sabree, Z.L. (2014) The crypt-dwelling primary bacterial symbiont of the polyphagous pentatomid pest Halyomorpha halys (Hemiptera: Pentatomidae). Environmental Entomology 43, 617–625.Google Scholar
Bigham, M. & Hosseininaveh, V. (2010) Digestive proteolytic activity in the pistachio green stink bug, Brachynema germari Kolenati (Hemiptera: Pentatomidae). Journal of Asia-Pacific Entomology 13, 221–227.Google Scholar
Bistolas, K.S.I., Sakamoto, R.I., Fernandes, J.A.M. & Goffredi, S.K. (2014) Symbiont polyphyly, co-evolution, and necessity in pentatomid stinkbugs from Costa Rica. Frontiers in Microbiology 5, 1–15.Google Scholar
Buchner, P. (1965) Endosymbiosis of Animals With Plant Microorganisms. New York, Mycological Society of America.Google Scholar
Douglas, A.E. (2013) Microbial brokers of insect-plant interactions revisited. Journal of Chemical Ecology 39, 952–961.Google Scholar
Engel, P. & Moran, N.A. (2013) The gut microbiota of insects - diversity in structure and function. FEMS Microbiology Reviews 37, 699–735.Google Scholar
Fierer, N. & Jackson, J. (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Applied and Environmental Microbiology 71, 4117.Google Scholar
Fukatsu, T. & Hosokawa, T. (2002) Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. Applied and Environmental Microbiology 68, 389–396.Google Scholar
Hayashi, T., Hosokawa, T., Meng, X.Y., Koga, R. & Fukatsu, T. (2015) Female-specific specialization of a posterior end region of the midgut symbiotic organ in Plautia splendens and allied stinkbugs. Applied and Environmental Microbiology 81, 2603–2611.Google Scholar
Hosokawa, T., Kikuchi, Y., Nikoh, N., Shimada, M. & Fukatsu, T. (2006) Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biology 4, 1841–1851.Google Scholar
Hosokawa, T., Kikuchi, Y., Shimada, M. & Fukatsu, T. (2007) Obligate symbiont involved in pest status of host insect. Proceedings of the Royal Society of London B: Biological Sciences 274, 1979–1984.Google Scholar
Hosokawa, T., Kikuchi, Y., Shimada, M. & Fukatsu, T. (2008) Symbiont acquisition alters behaviour of stinkbug nymphs. Biology Letters 4, 45–48.Google Scholar
Hosokawa, T., Hironaka, M., Inadomi, K., Mukai, H., Nikoh, N. & Fukatsu, T. (2013) Diverse strategies for vertical symbiont transmission among subsocial stinkbugs. PLoS ONE 8, 4–11.Google Scholar
Hosokawa, T., Hironaka, M., Mukai, H., Inadomi, K., Suzuki, N. & Fukatsu, T. (2012) Mothers never miss the moment: a fine-tuned mechanism for vertical symbiont transmission in a subsocial insect. Animal Behaviour 83, 293–300.Google Scholar
Hosokawa, T., Ishii, Y., Nikoh, N., Fujie, M., Satoh, N. & Fukatsu, T. (2016) Obligate bacterial mutualists evolving from environmental bacteria in natural insect populations. Nature Microbiology 1, 15011.Google Scholar
Kaltenpoth, M., Winter, S.A. & Kleinhammer, A. (2009) Localization and transmission route of Coriobacterium glomerans, the endosymbiont of pyrrhocorid bugs. FEMS Microbiology Ecology 69, 373–383.Google Scholar
Karamipour, N., Fathipour, Y. & Mehrabadi, M. (2016) Gammaproteobacteria as essential primary symbionts in the striped shield bug, Graphosoma lineatum (Hemiptera: Pentatomidae). Scientific Reports 6, 33168.Google Scholar
Kashkouli, M., Fathipour, Y. & Mehrabadi, M. (2018) Potential management tactics for pistachio stink bugs, Brachynema germari, Acrosternum heegeri and A. arabicum (hemiptera: Pentatomidae): high temperature and chemical surface sterilants leading to symbiont suppression. Journal of Economic Entomology 112(1), 244–254. doi: 10.1093/jee/toy324.Google Scholar
Kenyon, L.J., Meulia, T. & Sabree, Z.L. (2015) Habitat visualization and genomic analysis of “candidatus Pantoea carbekii,” the primary symbiont of the brown marmorated stink bug. Genome Biology and Evolution 7, 620–635.Google Scholar
Kikuchi, Y., Hosokawa, T. & Fukatsu, T. (2007) Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Applied and Environmental Microbiology 73, 4308–4316.Google Scholar
Kikuchi, Y., Hosokawa, T., Nikoh, N., Meng, X.-Y., Kamagata, Y. & Fukatsu, T. (2009) Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biology 7, 2.Google Scholar
Kikuchi, Y., Hosokawa, T., Nikoh, N. & Fukatsu, T. (2012) Gut symbiotic bacteria in the cabbage bugs Eurydema rugosa and Eurydema dominulus (Heteroptera: Pentatomidae). Applied Entomology and Zoology 47, 1–8.Google Scholar
Koga, R., Tsuchida, T. & Fukatsu, T. (2009) Quenching autofluorescence of insect tissues for in situ detection of endosymbionts. Applied Entomology and Zoology 44, 281–291.Google Scholar
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402–408.Google Scholar
Mehrnejad, M.R. (2001) The current status of pistachio pests in Iran. Cahiers Options Méditerranéennes 322, 315–322.Google Scholar
Mohammadpour, M., Ziaaddini, M., Jalali, M.A., Hashemirad, H. & Mohammadi-Khoramabadi, A. (2016) Egg parasitoids of the pistachio green stink bug, Brachynema germari (Hemiptera: Pentatomidae) in Kerman province, Iran. Zoology and Ecology 26, 28–34.Google Scholar
Moran, N.A., Dale, C., Dunbar, H., Smith, W.A. & Ochman, H. (2003) Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome. Environmental Microbiology 5, 116–126.Google Scholar
Moran, N.A., Russell, J.A., Koga, R. & Fukatsu, T. (2005) Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Applied and Environmental Microbiology 71, 3302–3310.Google Scholar
Moran, N.A., McCutcheon, J.P. & Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics 42, 165–190.Google Scholar
Pourkhatoon, S., Ziaaddini, M., Alizadeh, A., Jalali, M.A. & Ebrahimi, M. (2016) Biological characteristic of Brachynema germari (Hemiptera: Pentatomidae): comparative study of composite and natural diet. Journal of Economic Entomology 109, 1273–1282.Google Scholar
Prado, S.S. & Almeida, R.P.P. (2009 a) Phylogenetic placement of pentatomid stink bug gut symbionts. Current Microbiology 58, 64–69.Google Scholar
Prado, S.S. & Almeida, R.P.P. (2009 b) Role of symbiotic gut bacteria in the development of Acrosternum hilare and Murgantia histrionica. Entomologia Experimentalis et Applicata 132, 21–29.Google Scholar
Prado, S.S. & Zucchi, T.D. (2012) Host-symbiont interactions for potentially managing heteropteran pests. Psyche 2012, 1–9, Article ID 269473.Google Scholar
Prado, S.S., Hung, K.Y., Daugherty, M.P. & Almeida, R.P.P. (2010) Indirect effects of temperature on stink bug fitness, via maintenance of gut-associated symbionts. Applied and Environmental Microbiology 76, 1261–1266.Google Scholar
Ramzi, S. & Hosseininaveh, V. (2010) Biochemical characterization of digestive α -amylase, α -glucosidase and β -glucosidase in pistachio green stink bug, Brachynema germari Kolenati (Hemiptera: Pentatomidae). Journal of Asia-Pacific Entomology 13, 215–219.Google Scholar
Shigenobu, S., Watanabe, H., Hattori, M., Ishikawa, H. & sakaki, Y. (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407, 81–85.Google Scholar
Su, Q., Zhou, X. & Zhang, Y. (2013) Symbiont-mediated functions in insect hosts. Communicative and Integrative Biology 6, e23804.Google Scholar
Sudakaran, S., Salem, H., Kost, C. & Kaltenpoth, M. (2012) Geographical and ecological stability of the symbiotic mid-gut microbiota in European firebugs, pyrrhocoris apterus (Hemiptera, Pyrrhocoridae). Molecular Ecology 21, 6134–6151.Google Scholar
Sudakaran, S., Kost, C. & Kaltenpoth, M. (2017) Symbiont acquisition and replacement as a source of ecological innovation. Trends in Microbiology 25, 375–390.Google Scholar
Taylor, C.M., Coffey, P.L., DeLay, B.D. & Dively, G.P. (2014) The importance of gut symbionts in the development of the brown marmorated stink bug, halyomorpha halys (Stal). PLoS ONE 9, e90312.Google Scholar
Wernegreen, J.J. (2012) Mutualism meltdown in insects: bacteria constrain thermal adaptation. Current Opinion in Microbiology 15, 255–262.Google Scholar