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Bacterial communities associated with invasive populations of Bactrocera dorsalis (Diptera: Tephritidae) in China

  • L.J. Liu (a1), I. Martinez-Sañudo (a2), L. Mazzon (a2), C.S. Prabhakar (a1) (a3), V. Girolami (a2), Y.L. Deng (a4), Y. Dai (a1) and Z.H. Li (a1)...

Abstract

The oriental fruit fly Bactrocera dorsalis (Hendel) is a destructive insect pest of a wide range of fruits and vegetables. This pest is an invasive species and is currently distributed in some provinces of China. To recover the symbiotic bacteria of B. dorsalis from different invasion regions in China, we researched the bacterial diversity of this fruit fly among one laboratory colony (Guangdong, China) and 15 wild populations (14 sites in China and one site in Thailand) using DNA-based approaches. The construction of 16S rRNA gene libraries allowed the identification of 24 operational taxonomic units of associated bacteria at the 3% distance level, and these were affiliated with 3 phyla, 5 families, and 13 genera. The higher bacterial diversity was recovered in wild populations compared with the laboratory colony and in samples from early term invasion regions compared with samples from late term invasion regions. Moreover, Klebsiella pneumoniae and Providencia sp. were two of the most frequently recovered bacteria, present in flies collected from three different regions in China where B. dorsalis is invasive. This study for the first time provides a systemic investigation of the symbiotic bacteria of B. dorsalis from different invasion regions in China.

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* Author for correspondence Tel: 86 -10-62733000 Fax: 86-10-62733404 E-mail: lizh@cau.edu.cn

References

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Aketarawong, N., Bonizzoni, M., Thanaphum, S., Gomulski, L.M., Gasperi, G. & Malacrida, A.R. (2007) Inferences on the population structure and colonization process of the invasive oriental fruit fly, Bactrocera dorsalis (Hendel). Molecular Ecology 16, 35223532.
Andongma, A.A., Wan, L., Dong, Y.C., Li, P., Desneux, N., White, J.A. & Niu, C.Y. (2015) Pyrosequencing reveals a shift in symbiotic bacteria populations across life stages of Bactrocera dorsalis . Scientific Reports 5, 9470.
Ashelford, K.E., Chuzhanova, N.A., Fry, J.C., Jones, A.J., & Weightman, A.J. (2006) New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Applied Environmental Microbiology 72, 57345741.
Augustinos, A.A., Drosopoulou, E., Gariou-Papalexiou, A., Asimakis, E.D., Cáceres, C., Tsiamis, G., Bourtzis, K., Mavragani-Tsipidou, P. & Zacharopoulou, A. (2015) Cytogenetic and symbiont analysis of five members of the B. dorsalis complex (Diptera, Tephritidae): no evidence of chromosomal or symbiont-based speciation events. Zookeys 540, 273298.
Bohannan, B.J.M. & Hughes, J.B. (2003) New approaches to analyzing microbial biodiversity data. Current Opinion Microbiology 6, 282287.
Bai, Q. & Song, F.M. (1997) Report about the damage on mango and the prevention and control research of Bactrocera dorsalis . Tropical Agriculture Science (in Chinese) 4, 4548.
Behar, A., Yuval, B. & Jurkevitch, E. (2005) Enterobacteria-mediated nitrogen fixation in natural populations of the fruit fly Ceratitis capitata . Molecular Ecology 14, 26372643.
Behar, A., Jurkevitch, E. & Yuval, B. (2008 a) Bringing back the fruit into fruit fly-bacteria interactions. Molecular Ecology 17, 13751386.
Behar, A., Yuval, B. & Jurkevitch, E. (2008 b) Gut bacterial communities in the Mediterranean fruit fly (Ceratitis capitata) and their impact on host longevity. Journal of Insect Physiology 54, 13771383.
Behar, A., Yuval, B. & Jurkevitch, E. (2008 c) Community structure of the Mediterranean fruit fly microbiota: seasonal and spatial sources of variation. Israel Journal of Ecology and Evolution 54, 181191.
Ben-Yosef, M., Jurkevitch, E. & Yuval, B. (2008) Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata . Physiological Entomology 33, 145154.
Bextine, B., Lampe, D., Lauzon, C., Jackson, B. & Miller, T.A. (2005) Establishment of a genetically marked insect-derived symbiont in multiple host plants. Current Microbiology 50, 17.
Capuzzo, C., Firrao, G., Mazzon, L., Squartini, A. & Girolami, V. (2005) Candidatus Erwinia dacicola’, a coevolved symbiotic bacterium of the olive fly Bactrocera oleae (Gmelin). International Journal of Systematic Evolutionary Microbiology 55, 16411647.
Chao, A. (1984) Non-parametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11, 265270.
Clarke, A.R., Armstrong, K.F., Carmichael, A.E., Milne, J.R., Raghu, S., Roderick, G.K. & Yeates, D.K. (2005) Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. Annual Review of Entomology 50, 293319.
Feldhaar, H. (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecological Entomology 36, 533543.
Felsenstein, J. (1989) PHYLIP-Phylogeny Inference Package (version 3.2). Cladistics 5, 164166.
Himler, A.G., Adachi-Hagimori, T., Bergen, J.E., Kozuch, A., Kelly, S.E. & Tabashnik, B.E. (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332, 254256.
Jang, E.B. & Nishijima, K.A. (1990) Identification and attractancy of bacteria associated with Dacus dorsalis (Diptera, Tephritidae). Environmental Entomology 19, 17261731.
Konstantopoulou, M.A., Raptopoulos, D.G., Stavrakis, N.G. & Mazomenos, B.E. (2005) Microflora species and their volatile compounds affecting development of an alcohol dehydrogenase homozygous strain (Adh-I) of Bactrocera (Dacus) oleae (Diptera: Tephritidae). Journal of Economic Entomology 98, 19431949.
Kounatidis, I., Crotti, E., Sapountzis, P., Sacchi, L., Rizzi, A. & Chouaia, B. (2009) Acetobacter tropicalis Is a Major Symbiont of the Olive Fruit Fly (Bactrocera oleae). Applied Environmental Microbiology 75, 32813288.
Kuzina, L.V., Peloquin, J.J., Vacek, D.C. & Miler, T.A. (2001) Isolation and identification of bacteria associated with adult laboratory Mexican fruit flies, Anastrepha ludens (Diptera: Tephritidae). Current Microbiology 42, 290294.
Lauzon, C.R. (2003) Symbiotic relationships of Tephritids. pp. 115129 in Bourtzis, K. & Miller, T.A. (Eds) Insect Symbiosis. Boca Raton, FL, CRC Press.
Lauzon, C.R., Sjogren, R.E. & Prokopy, R.J. (2000) Enzymatic capabilities of bacteria associated with apple maggot flies: a postulated role in attraction. Journal of Chemical Ecology 26, 953967.
Lauzon, C.R., Bussert, T.G., Sjogren, R.E. & Prokopy, R.J. (2003) Serratia marcescens as a bacterial pathogen of Rhagoletis pomonella flies (Diptera: Tephritidae). European Journal of Entomology 100, 8792.
Li, H.X. & Ye, H. (2000) Infestation and distribution of the Oriental fruit fly (Diptera: Tephritidae) in Yunnan Province. Journal of Yunnan University 22, 473475 (In Chinese).
Li, W.F., Yang, L., Tang, K., Zeng, L. & Liang, G.W. (2007) Microsatellite polymorphism of Bactrocera dorsalis (Hendel) populations in China. Acta Entomologica Sinica 50, 12551262 (In Chinese).
Li, Y.L., Wu, Y., Chen, H., Wu, J.J. & Li, Z.H. (2012) Population structure and colonization of Bactrocera dorsalis (Diptera: Tephritidae) in China, inferred from mtDNA COI sequences. Journal of Applied Entomology 136, 241251.
Liu, J., Zhao, H., Jiang, K., Zhou, X.P. & Liu, S.S. (2009) Differential indirect effects of two plant viruses on an invasive and an indigenous whitefly vector: implications for competitive displacement. Annals of Applied Biology 155, 439448.
Lu, M., Zhou, X.D., De Beer, Z.W., Wingfield, M.J. & Sun, J.H. (2009) Ophiostomatoid fungi associated with the invasive pine-infesting bark beetle, Dendroctonus valens, in China. Fungal Diversity 38, 133145.
Mazzon, L., Piscedda, A., Simonato, M., Martinez-Sañudo, I., Squartini, A. & Girolami, V. (2008) Presence of specific symbiotic bacteria in flies of the subfamily Tephritinae (Diptera: Tephritidae) and their phylogenetic relationships: proposal of ‘Candidatus Stammerula tephritidis. International Journal of Systematic Evolutionary Microbiology 58, 12771287.
Mazzon, L., Martinez-Sanudo, I., Simonato, M., Squartini, A., Savio, C.& Girolami, V. (2010) Phylogenetic relationships between flies of the Tephritinae subfamily (Diptera, Tephritidae) and their symbiotic bacteria. Molecular Phylogenetics and Evolution 56, 312326.
Miyazaki, S., Boush, G.M. & Baerwald, R.J. (1968) Amino acid synthesis by pseudomonas melophthora bacterial symbiote of Rhagoletis pomonella (Diptera). Journal of Insect Physiology 14, 513518.
Morrow, J.L., Frommer, M., Shearman, D.C.A. & Riegler, M. (2015 a) The microbiome of field-caught and laboratory-adapted Australian tephritid fruit fly species with different host plant use and specialisation. Microbial Ecology 70, 498508.
Morrow, J.L., Frommer, M., Royer, J.E., Shearman, D.C.A. & Riegler, M. (2015 b) Wolbachia pseudogenes and low prevalence infections in tropical but not temperate Australian tephritid fruit flies: manifestations of lateral gene transfer and endosymbiont spillover? BMC Evolutionary Biology 15, 202218.
Rani, A., Sharma, A., Rajagopal, R., Adak, T. & Bhatnagar, R.K. (2009) Bacterial diversity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi-an Asian malarial vector. BMC Microbiology 9, 96.
Robacker, D.C. & Lauzon, C.R. (2002) Purine metabolizing capability of Enterobacter agglomerans affects volatiles production and attractiveness to Mexican fruit fly. Journal of Chemical Ecology 28, 15491563.
Robacker, D.C., Lauzon, C.R. & He, X.D. (2004) Volatiles production and attractiveness to the Mexican fruit fly of Enterobacter agglomerans isolated from apple maggot and Mexican fruit flies. Journal of Chemical Ecology 30, 13291347.
Robacker, D.C., Lauzon, C.R., Patt, J., Margara, F. & Sacchetti, P. (2009) Attraction of Mexican fruit flies (Diptera: Tephritidae) to bacteria: effects of culturing medium on odour volatiles. Journal of Applied Entomology 133, 155163.
Sacchetti, P., Granchietti, A., Landini, S., Viti, C., Giovannetti, L. & Belcari, A. (2008) Relationships between the olive fly and bacteria. Journal of Applied Entomology 132, 682689.
Schloss, P.D., Delalibera, I., Handelsman, J. & Raffa, K.F. (2006) Bacteria associated with the guts of two wood-boring beetles: Anoplophora glabripennis and Saperda vestita (Cerambycidae). Environmental Entomology 35, 625629.
Schutze, M.K., Mahmood, K., Pavasvici, A., Bo, W., Newman, J., Clarke, A.R., Krosch, M.N. & Cameron, S. (2015) One and the same: integrative taxonomic evidence that Bactrocera invadens (Diptera: Tephritidae) is the same species as the Oriental fruit fly Bactrocera dorsalis . Systematic Entomology 40, 472486.
Shi, W., Kerdelhue, C. & Ye, H. (2010) Population genetic structure of the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) from Yunnan province (China) and nearby sites across the border. Genetica 138, 377385.
Sun, X., Cui, L.W. & Li, Z.H. (2007) Diversity and Phylogeny of Wolbachia infecting Bactrocera dorsalis (Diptera:Tephritidae) populations from China. Environmental Entomology 36, 12831289.
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology Evolution 24, 15961599.
Tang, M., Lv, L., Jing, S.L., Zhu, L.L. & He, G.C. (2010) Bacterial symbionts of the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae). Applied Environmental Microbiology 76, 17401745.
Thao, M.L., Gullan, P.J. & Baumann, P. (2002) Secondary (Proteobacteria) endosymbionts infect the primary (gamma-) endosymbionts of mealybugs multiple times and coevolve with their hosts. Applied Environmental Microbiology 68, 31903197.
Tsiropoulos, G.J. (1983) Microflora associated with wild and laboratory reared adult olive fruit flies, Dacus oleae (Gmel). Journal of Applied Entomology 96, 337340.
Wang, H., Jin, L. & Zhang, H. (2011) Comparison of the diversity of the bacterial communities in the intestinal tract of adult Bactrocera dorsalis from three different populations. Journal of Applied Microbiology 110, 13901401.
Wang, H., Jin, L., Peng, T., Zhang, H., Chen, Q. & Hua, Y. (2014) Identification of cultivable bacteria in the intestinal tract of Bactrocera dorsalis from three different populations and determination of their attractive potential. Pest Management Science 70, 8087.
Zhou, G.L., Ye, J., Yuan, P. & Pan, S.H. (2006) The invasive mechanism of Bactrocera dorsalis in Shanghai. Plant Quarantine (in Chinese) 20, 4446.

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