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Characterization of the symbiont Rickettsia in the mirid bug Nesidiocoris tenuis (Reuter) (Heteroptera: Miridae)

Published online by Cambridge University Press:  25 July 2014

A. Caspi-Fluger ,
M. Inbar ,
S. Steinberg ,
Y. Friedmann ,
M. Freund ,
N. Mozes-Daube  and
E. Zchori-Fein
A. Caspi-Fluger
Affiliation:
Department of Entomology, Newe-Ya'ar Research Center, ARO, Ramat-Yishay 30095, Israel Department of Evolutionary and Environmental Biology, University of Haifa, Haifa 31905, Israel
M. Inbar
Affiliation:
Department of Evolutionary and Environmental Biology, University of Haifa, Haifa 31905, Israel
S. Steinberg
Affiliation:
BioBee Sde Eliyahu Ltd, Kibbutz Sde Eliyahu 10810, Israel
Y. Friedmann
Affiliation:
Bio-Imaging Unit, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel.
M. Freund
Affiliation:
BioBee Sde Eliyahu Ltd, Kibbutz Sde Eliyahu 10810, Israel
N. Mozes-Daube
Affiliation:
Department of Entomology, Newe-Ya'ar Research Center, ARO, Ramat-Yishay 30095, Israel
E. Zchori-Fein*
Affiliation:
Department of Entomology, Newe-Ya'ar Research Center, ARO, Ramat-Yishay 30095, Israel
*
*Author for correspondence Phone: +972-4-9539549 Fax: +972-4-9836936 E-mail: [email protected]
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Abstract

Nesidiocoris tenuis (Reuter) (Heteroptera: Miridae) is an omnivorous insect used for biological control. Augmentative release and conservation of N. tenuis have been used for pest control in tomato crops. Intracellular bacterial symbionts of arthropods are common in nature and have diverse effects on their hosts; in some cases they can dramatically affect biological control. Fingerprinting methods showed that the symbiotic complex associated with N. tenuis includes Wolbachia and Rickettsia. Rickettsia of N. tenuis was further characterized by sequencing the 16S rRNA and gltA bacterial genes, measuring its amount in different developmental stages of the insect by real-time polymerase chain reaction, and localizing the bacteria in the insect's body by fluorescence in situ hybridization. The Rickettsia in N. tenuis exhibited 99 and 96% similarity of both sequenced genes to Rickettsia bellii and Rickettsia reported from Bemisia tabaci, respectively. The highest amount of Rickettsia was measured in the 5th instar and adult, and the symbionts could be detected in the host gut and ovaries. Although the role played by Rickettsia in the biology of N. tenuis is currently unknown, their high amount in the adults and localization in the gut suggest that they may have a nutritional role in this insect.

Keywords

gut symbiontmicrobial communityomnivory
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 104 , Issue 6 , December 2014 , pp. 681 - 688
Copyright
Copyright © Cambridge University Press 2014 

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References

Abe, Y., Mishiro, K. & Takanashi, M. (1995) Symbiont of brown-winged green bug, Plautia stali Scott. Japanese Journal of Applied Entomology and Zoology 39, 109–115.CrossRefGoogle Scholar
Braig, H.R., Zhou, W., Dobson, S.L. & O'Neill, S.L. (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis . Journal of Bacteriology 180, 2373–2378.Google Scholar
Brumin, M., Levy, M. & Ghanim, M. (2012) Transovarial transmission of Rickettsia spp. and organ-specific infection of the whitefly Bemisia tabaci . Applied Environmental Microbiology Journal 78, 5565–5574.CrossRefGoogle ScholarPubMed
Buchner, P. (1965) Endosymbiosis of Animals with Plant Microorganisms. New York, Interscience Publishers.Google Scholar
Caspi-Fluger, A., Inbar, M., Mozes-Daube, N., Mouton, L., Hunter, M.S. & Zchori-Fein, E. (2011) Rickettsia ‘in’ and ‘out’: two different localization patterns of a bacterial symbiont in the same insect species. PLoS ONE 6, e21096.Google Scholar
Caspi-Fluger, A., Inbar, M., Mozes-Daube, N., Katzir, N., Portnoy, V., Belausov, E., Hunter, M.S. & Zchori-Fein, E. (2012) Horizontal transmission of the insect symbiont Rickettsia is plant mediated. Proceedings of the Royal Society of London B 279, 1791–1796.Google Scholar
Castañé, C., Arnó, J., Gabarra, R. & Alomar, O. (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biological Control 59, 22–29.CrossRefGoogle Scholar
Chang, K.P. & Musgrave, A.J. (1970). Ultrastructure of Rickettsia-like microorganisms in the midgut of a plant bug, Stenotus binotatus Jak. (Heteroptera: Miridae). Canadian Journal of Microbiology 16, 621–622.Google Scholar
Chiel, E., Zchori-Fein, E., Inbar, M., Gottlieb, Y., Adachi-Hagimori, T., Kelly, S.E., Asplen, M.K. & Hunter, M.S. (2009) Almost there: transmission routes of bacterial symbionts between trophic levels. PLoS ONE 4, e4767.CrossRefGoogle ScholarPubMed
Fournier, P.E., Roux, V. & Raoult, D. (1998) Phylogenetic analysis of spotted fever group Rickettsiae by study of the outer surface protein rOmpA. International Journal of Systematic Bacteriology 48, 839–849.CrossRefGoogle ScholarPubMed
Fournier, P.E., Dumler, J.S., Greub, G., Zhang, J., Yimin, W. & Raoult, D. (2003) Gene sequence-based criteria for the identification of new Rickettsia isolates and description of Rickettsia heilongjiangensis sp. nov. Journal of Clinical Microbiology 41, 5456–5465.CrossRefGoogle ScholarPubMed
Frohlich, D.R., Torres-Jerez, I., Bedford, I.D., Markham, P.G. & Brown, J.K. (1999) A phylogeographical analysis of the Bemisia tabaci species complex based on mitochondrial DNA markers. Molecular Ecology 8, 1683–1691.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Glasgow, H. (1914) The gastric caeca and the caecal bacteria of the Heteroptera. Biological Bulletin 26, 101–170.Google Scholar
Gottlieb, Y., Ghanim, M., Chiel, E., Gerling, D., Portnoy, V., Steinberg, S., Tzuri, G., Horowitz, R.A., Belausov, E., Mozes-Daube, N., Kontsedalov, S., Gershon, M., Gal, S., Katzir, N. & Zchori-Fein, E. (2006) Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Applied and Environmental Microbiology 72, 3646–3652.CrossRefGoogle ScholarPubMed
Gottlieb, Y., Perlman, S.J., Chiel, E. & Zchori-Fein, E. (2011) Rickettsia get around. pp. 191–206 in Zchori-Fein, E. & Bourtzis, K. (Eds). Manipulative Tenants—Bacteria Associated with Arthropods. Boca Raton, FL, CRC Press.Google Scholar
Haas, F. & König, H. (1987) Characterisation of an anaerobic symbiont and the associated aerobic bacterial flora of Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). FEMS Microbiology Letters 45, 99–106.CrossRefGoogle Scholar
Hosokawa, T., Kikuchi, Y., Meng, X.-Y. & Fukatsu, T. (2005) The making of symbiont capsule in the plataspid stinkbug Megacopta punctatissima . FEMS Microbiology Ecology 54, 471–477.Google Scholar
Hosokawa, T., Kikuchi, Y., Nikon, N., Meng, X-Y., Hironaka, M. & Fukatsu, T. (2010) Phylogenetic position and peculiar genetic traits of a midgut bacterial symbiont of the stinkbug Parastrachia japonensis . Applied and Environmental Microbiology 76, 4130–4135.Google Scholar
Huber-Schneider, L. (1957) Morphologische und physiologische Untersuchungen an der Wanze Mesocerus marginatus L. und ihren Symbionten (Heteroptera). Zeitschrift für Morphologie und Ökologie der Tiere 46, 433–480.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
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.CrossRefGoogle ScholarPubMed
Kikuchi, Y., Hosokawa, T. & Fukatsu, T. (2011) An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME Journal 5, 446–460.CrossRefGoogle ScholarPubMed
Kikuchi, Y., Hayatsu, M., Hosokawa, T., Nagayama, A., Tago, K. & Fukatsu, T. (2012) Symbiont-mediated insecticide resistance. Proceedings of the National Academic of Sciences of the USA 109, 8618–8622.Google Scholar
Kuechler, S.M., Renz, P., Dettner, K. & Kehl, S. (2012) Diversity of symbiotic organs and bacterial endosymbionts of lygaeoid bugs of the families Blissidae and Lygaeidae (Hemiptera: Heteroptera: Lygaeoidea). Applied and Environmental Microbiology 78, 2648–2659.CrossRefGoogle ScholarPubMed
Machtelinckx, T., Van Leeumen, T., Vanholme, B., Gehesquiere, B., Dermauw, W., Vandekerkhove, B., Gheysen, G. & De Clercq, P. (2009) Wolbachia induces strong cytoplasmic incompatibility in the predatory bug Macrolophus pygmaeus . Insect Molecular Biology 18, 373–381.CrossRefGoogle ScholarPubMed
Machtelinckx, T., Van Leeumen, T., Van De Wiele, T., Boon, N., De Vos, W., Sanchez, J-A., Nannini, M., Gheysen, G. & De Clercq, P. (2012) Microbial community of predatory bugs of the genus Macrolophus (Hemiptera: Miridae). BMC Microbiology 12, S9.CrossRefGoogle ScholarPubMed
Matsuura, Y., Kikuchi, Y., Hosokawa, T., Koga, R., Meng, X.-Y., Kamagata, Y., Nikoh, N. & Fukatsu, T. (2012) Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs. ISME Journal 6, 397–409.CrossRefGoogle ScholarPubMed
Muyzer, G., Hottentrager, S., Teske, A. & Wawer, C. (1996) Denaturing gradient gel electrophoresis of PCR amplified 16 s rDNA – a new molecular approach to analyze the genetic diversity of mixed microbial communities. pp. 1–23 in Akkermans, A.D.L., van Elsas, J.D. & de Bruijn, F.J. (Eds) Molecular Microbial Ecology Manual 3.4.4. Dordrecht, The Netherlands, Kluwer Academic Publishers.Google Scholar
Nikoh, N., Hosokawa, T., Oshima, K., Hattori, M. & Fukatsu, T. (2011) Reductive evolution of bacterial genome in insect gut environment. Genome Biology and Evolution 3, 702–714.Google Scholar
Prado, S. & Almeida, R.P.P. (2009) 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., Rubinoff, D. & Almeida, R.P.P. (2006) Vertical transmission of a pentatomid caeca-associated symbiont. Annals of the Entomological Society of America 99, 577–585.CrossRefGoogle Scholar
Perdikis, D., Fantinou, A. & Lykouressis, D. (2011) Enhancing pest control in annual crops by conservation of predatory Heteroptera. Biological Control 59, 13–21.Google Scholar
Sakurai, M., Koga, R., Tsuchida, T., Meng, X.-Y. & Fukatsu, T. (2005) Rickettsia symbiont in the pea aphid Acyrthosiphon pisum: novel cellular tropism, effect on host fitness, and interaction with the essential symbiont Buchnera . Applied and Environmental Microbiology 71, 4069–4075.CrossRefGoogle ScholarPubMed
Salem, H., Kreutzer, E., Sudakaran, S. & Kaltenpoth, M. (2013) Actinobacteria as essential symbionts in firebugs and cotton stainers (Hemiptera, Pyrrhocoridae). Environmental Microbiology 15, 1956–1968.Google Scholar
Sanchez, J.A. & Lacasa, A. (2008) Impact of the zoophytophagous plant bug Nesidiocoris tenuis (Heteroptera: Miridae) on tomato yield. Journal of Economic Entomology 101, 1864–1870.Google Scholar
Sanchez, J.A., Martinez-Cascales, J.I. & Lacasa, A. (2003) Abundance and wild host plants of predator mirids (Heteroptera: Miridae) in horticultural crops in the Southeast of Spain. IOBC WPRS Bulletin 26, 147–151.Google Scholar
Tada, A., Kikuchi, Y., Hosokawa, T., Musolin, D.L., Fujisaki, K. & Fukatsu, T. (2011) Obligate association with gut bacterial symbiont in Japanese populations of the southern green stinkbug Nezara viridula (Heteroptera: Pentatomidae). Applied Entomology and Zoology 46, 483–488.Google Scholar
Tavella, L. & Goula, M. (2001) Dicyphini collected in horticultural areas of north-western Italy (Heteroptera: Miridae). Bollettino di Zoologia Agraria e di Bachicoltura 33, 93–102.Google Scholar
Urbaneja, A., Gervasio, T. & Stansly, P. (2005) Influence of host plant and prey availability on developmental time and survivorship of Nesidiocoris tenuis (Het.: Miridae). Biocontrol Science and Technology 15, 513–518.CrossRefGoogle Scholar
van Lenteren, J. (2011) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57, 1–20.CrossRefGoogle Scholar
Weinert, L., Werren, J., Aebi, A., Stone, G. & Jiggins, F.M. (2009) Evolution and diversity of Rickettsia bacteria. BMC Biology 7, 6.Google Scholar
Weisburg, W.G., Barns, S.M., Pellelier, D.A. & Lane, D.J. (1991) 16S ribosomal DNA amplification for phylogenetic study. Journal Bacteriology 173, 697–703.Google Scholar
Wheeler, A.G. Jr. (2001) Biology of the Plant Bugs (Hemiptera: Miridae): Pests, Predators, Opportunists. Ithaca, NY, Cornell University Press.Google Scholar
Zchori-Fein, E. & Bourtzis, K. (2011) Manipulative Tenants – Bacteria Associated with Arthropods. Boca Raton, FL, CRC Press.Google Scholar
Zindel, R., Gottlieb, Y. & Aebi, A. (2011) Arthropod symbioses: a neglected parameter in pest- and disease-control programmes. Journal of Applied Ecology 48, 864–872.CrossRefGoogle Scholar