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Superinfection of five Wolbachia in the alnus ambrosia beetle, Xylosandrus germanus (Blandford) (Coleoptera: Curuculionidae)

Published online by Cambridge University Press:  24 August 2009

Y. Kawasaki ,
M. Ito ,
K. Miura  and
H. Kajimura
Y. Kawasaki*
Affiliation:
Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Aichi, 464-8601, Japan
M. Ito
Affiliation:
Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Aichi, 464-8601, Japan
K. Miura
Affiliation:
National Agricultural Research Center for Western Region, Fukuyama, Hiroshima, 721-8514, Japan Graduate School of Biosphere Science, Hiroshima University, Higashi-Hiroshima, Hiroshima, 739-8528, Japan
H. Kajimura
Affiliation:
Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Aichi, 464-8601, Japan
*
*Author for correspondence Fax: +81-52-789-5518 E-mail: [email protected]
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Abstract

Wolbachia bacteria are among the most common endosymbionts in insects. In Wolbachia research, the Wolbachia surface protein (wsp) gene has been used as a phylogenetic tool, but relationships inferred by single-locus analysis can be unreliable because of the extensive genome recombination among Wolbachia strains. Therefore, a multilocus sequence typing (MLST) method for Wolbachia, which relies upon a set of five conserved genes, is recommended. In this study, we examined whether the alnus ambrosia beetle, Xylosandrus germanus (Blandford), is infected with Wolbachia using wsp and MLST genes. Wolbachia was detected from all tested specimens of X. germanus (n=120) by wsp amplification. Five distinct sequences (i.e. five alleles) for wsp were found, and labeled as wXge1–5. MLST analysis and molecular phylogeny of concatenated sequences of MLST genes identified wXge3 and wXge5 as closely-related strains. The detection rate of wXge4 and wXge1 was 100% and 63.3%, respectively; wXge2, wXge3 and wXge5 were detected from less than 15% of specimens. We performed mitochondrial haplotype analyses that identified three genetic types of X. germanus, i.e. Clades A, B and C. Wsp alleles wXge1, wXge2 and wXge4 were detected in all clade A beetles; wXge2 allele was absent from Clades B and C. We concluded that (i) five wsp alleles were found from X. germanus, (ii) use of MLST genes, rather than the wsp gene, are more suited to construct Wolbachia phylogenies and (iii) wsp alleles wXge2 and wXge3/wXge5 would infect clade A and clade B/C of X. germanus, respectively.

Keywords

endosymbiotic bacteriaScolytinaemultilocus sequence typing methodmultiple infectionsinfection polymorphism
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 100 , Issue 2 , April 2010 , pp. 231 - 239
Copyright
Copyright © Cambridge University Press 2009

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References

Arthofer, A., Riegler, M., Avtzis, D.N. & Stauffer, C. Evidence for low-titre infections in insect symbiosis: Wolbachia in the bark beetle Pityogenes chalcographus (Coleoptera, Scolytinae) (p). Environmental Microbiology, in press (doi: 10.1111/j.1462-2920.2009.01914.x).Google Scholar
Baldo, L. & Werren, J.H. (2007) Revisiting Wolbachia supergroup typing based on WSP: Spurious lineages and discordance with MLST. Current Microbiology 55, 81–87.CrossRefGoogle ScholarPubMed
Baldo, L., Lo, N. & Werren, J.H. (2005) Mosaic nature of the Wolbachia surface protein. Journal of Bacteriology 187, 5406–5418.CrossRefGoogle ScholarPubMed
Baldo, L., Hotopp, J., Jolley, K., Bordenstein, S., Biber, S., Choudhury, R., Hayashi, C., Maiden, M., Tettelin, H. & Werren, J.H. (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Applied and Environmental Microbiology 72, 7098–7110.CrossRefGoogle ScholarPubMed
Baldo, L., Prendini, L., Corthals, A. & Werren, J.H. (2007) Wolbachia are present in southern African scorpions and cluster with supergroup F. Current Microbiology 55, 367–373.CrossRefGoogle ScholarPubMed
Baldo, L., Ayoub, N.A., Hayashi, C.Y., Russell, J.A., Stahlhut, J.K. & Werren, J.H. (2008) Insight into the routes of Wolbachia invasion: high levels of horizontal transfer in the spider genus Agelenopss revealed by Wolbachia strain and mitochondrial DNA diversity. Molecular Ecology 17, 557–569.CrossRefGoogle ScholarPubMed
Beaver, R. (1989) Insect-fungus relationships in the bark and ambrosia beetle. pp. 121–143 in Wilding, N., Collins, N., Hammond, P. & Weber, J. (Eds) Insect-Fungus Interaction. New York, NY, USA, Chapman and Hall.CrossRefGoogle Scholar
Breeuwer, J., Stouthamer, R., Barns, S., Pelletier, D., Weisburg, W. & Werren, J.H. (1992) Phylogeny of cytoplasmic incompatibility micro-organisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16S ribosomal DNA sequences. Insect Molecular Biology 1, 25–36.CrossRefGoogle ScholarPubMed
Dedeine, F., Ahrens, M., Calcaterra, L. & Shoemaker, D. (2005) Social parasitism in fire ants (Solenopsis spp.): a potential mechanism for interspecies transfer of Wolbachia. Molecular Ecology 14, 1543–1548.CrossRefGoogle ScholarPubMed
Farrell, B.D., Sequeira, A.S., O'Meara, B.C., Normark, B.B., Chung, J.H. & Jordal, B.H. (2001) The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55, 2011–2027.Google Scholar
Felsenstein, J. (2004) PHYLIP ver. 3.6: Phylogeny Inference Package. Seattle, WA, USA, University of Washington. http://evolution.gs.washington.edu/phylip.html.Google Scholar
Gotoh, T., Noda, H. & Ito, S. (2007) Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98, 13–20.CrossRefGoogle ScholarPubMed
Hall, T. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A. & Werren, J.H. (2008) How many species are infected with Wolbachia? – A statistical analysis of current data. FEMS Microbiology Letters 281, 215–220.CrossRefGoogle Scholar
Hoffmann, A.A. & Turelli, M. (1997) Cytoplasmic incompatibility in insects. pp. 42–80 in O'Neill, S.L., Hoffmann, A.A. & Werren, J.H. (Eds) Influential passengers: Inherited microorganisms and arthropod reproduction. Oxford, UK, Oxford University Press.CrossRefGoogle Scholar
Holden, P., Brookfield, J. & Jones, P. (1993) Cloning and characterization of an ftsZ homologue from a bacterial symbiont of Drosophila melanogaster. Molecular and General Genetics 240, 213–220.CrossRefGoogle ScholarPubMed
Hotopp, J.C., Clark, M., Oliveira, D., Foster, J., Fischer, P., Torres, M., Giebel, J., Kumar, N., Ishmael, N., Wang, S., Ingram, J., Nene, R., Shepard, J., Tomkins, J., Richards, S., Spiro, D., Ghedin, E., Slatko, B., Tettelin, H. & Werren, J.H. (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 1753–1756.CrossRefGoogle Scholar
Ito, M., Kajimura, H., Hamaguchi, K., Araya, K. & Lakatos, F. (2008) Genetic structure of Japanese populations of an ambrosia beetle, Xylosandrus germanus (Curculionidae: Scolytinae). Entomological Science 11, 375–383.CrossRefGoogle Scholar
Jamnongluk, W., Kittayapong, P., Baimai, V. & O'Neill, S. (2002) Wolbachia infections of tephritid fruit flies: molecular evidence for five distinct strains in a single host species. Current Microbiology 45, 255–260.CrossRefGoogle Scholar
Jolley, K., Feil, E., Chan, M. & Maiden, M. (2001) Sequence type analysis and recombinational tests (START). Bioinformatics 17, 1230–1231.CrossRefGoogle ScholarPubMed
Kaneko, T. (1965) Biology of some scolytid ambrosia beetles attacking tea plants. I. growth and development of two species of scolytid beetles reared on sterilized tea plants. Japanese Journal of Applied Entomology and Zoology 9, 211–216.CrossRefGoogle Scholar
Kirkendall, L. (1983) The evolution of mating systems in bark and ambrosia beetles (Coleoptera Scolytidae and Platypodidae). Zoological Journal of the Linnean Society 77, 293–352.CrossRefGoogle Scholar
Kirkendall, L. (1993) Ecology and evolution of biased sex ratios in bark and ambrosia beetles. pp. 235–345 in Wrensch, D. & Ebbert, M. (Eds) Evolution and Diversity of Sex Ratio in Insects and Mites. New York, NY, USA, Chapman and Hall.CrossRefGoogle Scholar
Kondo, N., Ijichi, N., Shimada, M. & Fukatsu, T. (2002a) Prevailing triple infection with Wolbachia in Callosobruchus chinensis (Coleoptera: Bruchidae). Molecular Ecology 11, 167–180.CrossRefGoogle ScholarPubMed
Kondo, N., Nikoh, N., Ijichi, N., Shimada, M. & Fukatsu, T. (2002b) Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proceedings of the National Academy of Sciences of the United States of America 99, 14280–14285.CrossRefGoogle Scholar
Kumar, S., Tamura, K. & Nei, M. (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.CrossRefGoogle ScholarPubMed
Malloch, G., Fenton, B. & Butcher, R. (2000) Molecular evidence for multiple infections of a new subgroup of Wolbachia in the European raspberry beetle Byturus tomentosus. Molecular Ecology 9, 77–90.CrossRefGoogle ScholarPubMed
Maiden, M.C., Bygraves, J.S., Feil, E., Morelli, G., Russell, J.E., Urwin, R., Zhang, Q., Zhou, J., Zurth, K., Caugant, D.A., Feavers, I.M., Achtman, M. & Spratt, B.G. (1998) Multilocus sequence typing: A portable approach to the identification of clones within populations of pathogenic microorganisms. Proceedings of the National Academy of Sciences of the United States of America 95, 3140–3145.CrossRefGoogle Scholar
Narita, S., Shimajiri, Y. & Nomura, M. (2009) Strong cytoplasmic incompatibility and high vertical transmission rate can explain the high frequencies of Wolbachia infection in Japanese populations of Colias erate poliographus (Lepidoptera: Pieridae). Bulletin of Entomological Research 99, 385–391.CrossRefGoogle ScholarPubMed
Nobuchi, A. (1985) Check-list of Coleoptera of Japan. Family Scolytidae. The Coleopterists' Association of Japan 30, 1–32.Google Scholar
Normark, B.B., Jordal, B.H. & Farrell, B.D. (1999) Origin of a haplodiploid beetle lineage. Proceedings of the Royal Society of London, Series B: Biological Sciences 266, 2253–2259.CrossRefGoogle Scholar
O'Neill, S., Giordano, R., Colbert, A., Karr, T. & Robertson, H. (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proceedings of the National Academy of Sciences of the United States of America 89, 2699–2702.CrossRefGoogle ScholarPubMed
O'Neill, S., Hoffmann, A. & Werren, J.H. (1997) Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. 214 pp. New York, NY, USA, Oxford University Press.CrossRefGoogle Scholar
Peer, K. & Taborsky, M. (2004) Female ambrosia beetles adjust their offspring sex ratio according to outbreeding opportunities for their sons. Journal of Evolutionary Biology 17, 257–264.CrossRefGoogle ScholarPubMed
Peer, K. & Taborsky, M. (2005) Outbreeding depression, but no inbreeding depression in haplodiploid ambrosia beetles with regular sibling mating. Evolution 59, 317–323.Google ScholarPubMed
Raychoudhury, R., Baldo, L., Oliveira, D.C. & Werren, J.H. (2009) Modes of Acquisition of Wolbachia: horizontal transfer, hybrid introgression and codivergence in the Nasonia species. Evolution 63, 165–183.CrossRefGoogle ScholarPubMed
Reuter, M. & Keller, L. (2003) High levels of multiple Wolbachia infection and recombination in the ant Formica exsecta. Molecular Biology and Evolution 20, 748–753.CrossRefGoogle ScholarPubMed
Rudinsky, J.A. (1962) Ecology of Scolytidae. Annual Review in Entomology 7, 327–348.CrossRefGoogle Scholar
Stauffer, C., van Meer, M. & Riegler, M. (1997) The presence of the proteobacteria Wolbachia in European Ips typographus (Col., Scolytidae) populations and the consequences for genetic data. Mitteilungen der Deutschen Gesellschaft fur Allgemeine und Angewandte Entomologie 11, 709–711.Google Scholar
Thompson, J., Higgins, D. & Gibson, T. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Vavre, F., Fleury, F., Lepetit, D., Fouillet, P. & Boulétreau, M. (1999) Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Molecular Biology and Evolution 16, 1711–1723.CrossRefGoogle ScholarPubMed
Vega, F., Benavides, P., Stuart, J. & O'Neill, S. (2002) Wolbachia infection in the coffee berry borer (Coleoptera: Scolytidae). Annals of the Entomological Society of America 95, 374–378.CrossRefGoogle Scholar
Werren, J.H. & Bartos, J.D. (2001) Recombination in Wolbachia. Current Biology 11, 431–435.CrossRefGoogle ScholarPubMed
Werren, J.H., Zhang, W. & Guo, L. (1995) Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proceedings of the Royal Society of London, Series B: Biological Series 261, 55–63.Google ScholarPubMed
Zabalou, S., Apostolaki, A., Pattas, S., Veneti, Z., Paraskevopoulos, C., Livadaras, I., Markakis, G., Brissac, T., Mercot, H. & Bourtzis, K. (2008) Multiple rescue factors within a Wolbachia strain. Genetics 178, 2145–2160.CrossRefGoogle ScholarPubMed
Zchori-Fein, E., Borad, C. & Harari, A. (2006) Oogenesis in the date stone beetle, Coccotrypes dactyliperda, depends on symbiotic bacteria. Physiological Entomology 31, 164–169.CrossRefGoogle Scholar
Zhou, W., Rousset, F. & O'Neil, S. (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proceedings of the Royal Society of London, Series B: Biological Sciences 265, 509–515.CrossRefGoogle ScholarPubMed
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