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Analyses of the gut bacteriomes of four important Drosophila pests

Published online by Cambridge University Press:  30 September 2021

Qingcai Lin ,
Yifan Zhai Open the ORCID record for Yifan Zhai [Opens in a new window] ,
Hao Chen ,
Dongyun Qin ,
Li Zheng  and
Huanhuan Gao
Qingcai Lin
Affiliation:
Institute of Plant Protection, Shandong Academy of Agricultural Sciences, Jinan, 250100, China
Yifan Zhai*
Affiliation:
Institute of Plant Protection, Shandong Academy of Agricultural Sciences, Jinan, 250100, China
Hao Chen
Affiliation:
Institute of Plant Protection, Shandong Academy of Agricultural Sciences, Jinan, 250100, China
Dongyun Qin
Affiliation:
Institute of Plant Protection, Shandong Academy of Agricultural Sciences, Jinan, 250100, China
Li Zheng
Affiliation:
Institute of Plant Protection, Shandong Academy of Agricultural Sciences, Jinan, 250100, China
Huanhuan Gao*
Affiliation:
Institute of Plant Protection, Shandong Academy of Agricultural Sciences, Jinan, 250100, China Shandong Academy of Grape, Jinan, 250100, China
*
*Corresponding authors. Emails: zyifan@tom.com; gaohuanhuan368@126.com
*Corresponding authors. Emails: zyifan@tom.com; gaohuanhuan368@126.com
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Abstract

Several Drosophila species (Diptera: Drosophilidae) have become serious economic pests of berry and soft-skinned stone fruits around the world. Prominent examples are Drosophila suzukii (Matsumura), D. melanogaster (Meigen), D. hydei (Sturtevant), and D. immigrans (Sturtevant). Information on the biology and ecology of Drosophila is important for a better understanding of these important fruit pests and, ultimately, for fruit protection. In this study, the gut bacteriomes of these four Drosophila species were surveyed and the differences among bacterial communities were characterised. The 16S rRNA genes of gut microbes were sequenced by Illumina MiSeq technology (Illumina, San Diego, California, United States of America), followed by α-diversity and β-diversity analyses. The results show that bacteria of the family Enterobacteriaceae (Kluyvera and Providencia; phylum Proteobacteria) dominated all four Drosophila species. Specific dominant gut bacterial communities were found in each Drosophila species. The dominant families in D. melanogaster and D. suzukii were Enterobacteriaceae, Comamonadaceae, and Acetobacteraceae. In the intestine of D. hydei, Enterobacteriaceae had a proportion of 56.99%, followed by Acetobacteraceae, Spiroplasmataceae, and Bacillales Incertae Sedis XII. In D. immigrans, besides Enterobacteriaceae, Alcaligenaceae, Flavobacteriaceae, Xanthomonadaceae, Comamonadaceae, and Sphingobacteriaceae also had high relative abundance. These data expand current knowledge about the putative function related to gut microbes – for example, the metabolism of carbohydrates, amino acids, inorganic ions, lipids, and secondary metabolites. This knowledge provides a basis for further metatranscriptomic and metaproteomic investigations.

Type
Research Paper
Information
The Canadian Entomologist , Volume 153 , Issue 6 , December 2021 , pp. 757 - 773
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Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada

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Footnotes

Subject Editor: Chris Keeling

References

Adair, K.L., Wilson, M., Bost, A., and Douglas, A.E. 2018. Microbial community assembly in wild populations of the fruit fly, Drosophila melanogaster . The ISME Multidisciplinary Journal of Microbial Ecology, 12: 959–972. https://doi.org/10.1038/s41396-017-0020-x.Google Scholar
Atallah, J., Teixeira, L., Salazar, R., Zaragoza, G., and Kopp, A. 2014. The making of a pest: the evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species. Proceedings of the Royal Society of London B: Biological Sciences, 281: 20132840. https://doi.org/10.1098/rspb.2013.2840.Google ScholarPubMed
Becher, P.G., Flick, G., Rozpędowska, E., Schmidt, A., Hagman, A., Lebreton, S., and Bengtsson, M. 2012. Yeast, not fruit volatiles, mediate Drosophila melanogaster attraction, oviposition and development. Functional Ecology, 26: 822–828. https://doi.org/10.1111/j.1365-2435.2012.02006.x.CrossRefGoogle Scholar
Bing, X., Gerlach, J., Loeb, G., and Buchon, N. 2018. Nutrient-dependent impact of microbes on Drosophila suzukii development. mBio, 9: e02199–17. https://doi.org/10.1128/mBio.02199-17.CrossRefGoogle ScholarPubMed
Bonwitt, J.H., Tran, M., Dykstra, E.A., Eckmann, K., Bell, M.E., Leadon, M., and Glover, W.A. 2018. Fly reservoir associated with Wohlfahrtiimonas bacteremia in a human. Emerging Infectious Diseases, 24: 370–373. https://doi.org/10.3201/eid2402.170913.CrossRefGoogle ScholarPubMed
Broderick, N.A. and Lemaitre, B. 2012. Gut-associated microbes of Drosophila melanogaster . Gut Microbes, 3: 307–321. https://doi.org/10.4161/gmic.19896.CrossRefGoogle ScholarPubMed
Chandler, J.A., James, P.M., Jospin, G., and Lang, J.M. 2014. The bacterial communities of Drosophila suzukii collected from undamaged cherries. Peer J, 2: e474. https://doi.org/10.1128/mBio.02199-17.CrossRefGoogle ScholarPubMed
Chandler, J.A., Morgan, L.J., Bhatnagar, S., Eisen, J.A., and Kopp, A. 2011. Bacterial Communities of diverse Drosophila species: ecological context of a host–microbe model system. PLOS Genetics, 7: e1002272. https://doi.org/10.1371/journal.pgen.1002272.CrossRefGoogle ScholarPubMed
Di Fiore, S. and Del Gallo, M. 1995. Endophytic bacteria: their possible role in the host plant. In Azospirillum VI and related microorganisms. Edited by Fendrik, I., del Gallo, M., Vanderleyden, J., and de Zamaroczy, M.. Volume 37. NATO ASI Series/Series G: Ecological Sciences. Springer, Berlin, Heidelberg, Germany. Pp. 169–187. https://doi.org/10.1007/978-3-642-79906-8_18.CrossRefGoogle Scholar
Dillon, R.J., Vennard, C.T., Buckling, A., and Charnley, A. 2005. Diversity of locust gut bacteria protects against pathogen invasion. Ecology Letters, 8: 1291–1298. https://doi.org/10.1111/j.1461-0248.2005.00828.x.CrossRefGoogle Scholar
Douglas, A.E. 2017. The B vitamin nutrition of insects: the contributions of diet, microbiome and horizontally acquired genes. Current Opinion in Insect Science, 23: 65–69. https://doi.org/10.1016/j.cois.2017.07.012.CrossRefGoogle Scholar
Douglas, A.E. 2018. The Drosophila model for microbiome research. Laboratory Animals, 47: 157–164. https://doi.org/10.1038/s41684-018-0065-0.CrossRefGoogle ScholarPubMed
Duplais, C., Sarou-Kanian, V., Massiot, D., Hassan, A., and Moreau, C.S. 2021. Gut bacteria are essential for normal cuticle development in herbivorous turtle ants. Nature Communications, 12: 1–5. https://doi.org/10.1038/s41467-021-21065-y.CrossRefGoogle ScholarPubMed
Fraune, S. and Bosch, T.C.G. 2010. Why bacteria matter in animal development and evolution. Bioessays, 32: 571–580. https://doi.org/10.1002/bies.200900192.CrossRefGoogle ScholarPubMed
Gao, H.H., Zhu, G.P., Lv, Z.Y., Yang, L.Y., Liu, S., and Wang, Y.M. 2018. Dynamic regularity of Drosophila among different grape varieties. Sino-Overseas Grapevine & Wine, 1: 20–25.Google Scholar
Goodhue, R.E., Rolda, M., and Farnsworth, D. 2011. Spotted-wing Drosophilia infestation of California strawberries and raspberries: economic analysis of potential revenue losses and control costs. Pest Management Science, 67: 1396–1402. https://doi.org/10.1002/ps.2259.CrossRefGoogle Scholar
Gupta, A.K., Nayduch, D., Verma, P., Shah, B., Ghate, H.V., and Patole, M.S. 2012. Phylogenetic characterisation of bacteria in the gut of house flies (Musca domestica L.). FEMS Microbiology Ecology, 9: 581–593.10.1111/j.1574-6941.2011.01248.xCrossRefGoogle Scholar
Katoh, T., Nakaya, D., Tamura, K., and Aotsuka, T. 2007. Phylogeny of the Drosophila immigrans species group (Diptera: Drosophilidae) based on Adh and Gpdh sequences. Zoological Science, 24: 913–921. https://doi.org/10.2108/zsj.24.913.CrossRefGoogle ScholarPubMed
Kumar, D., Sun, Z., Cao, G., Xue, R., Hu, X., and Gong, C. 2019. Study of gut bacterial diversity of Bombyx mandarina and Bombyx mori through 16S rRNA gene sequencing. Journal of Asia–Pacific Entomology, 22: 522–530. https://doi.org/10.1016/j.aspen.2019.03.005.CrossRefGoogle Scholar
Lee, J.K., Lee, Y.Y., Park, K.H., Sim, J., Choi, Y., and Lee, S.J. 2014. Wohlfahrtiimonas larvae sp. nov., isolated from the larval gut of Hermetia illucens (Diptera: Stratiomyidae). Antonie van Leeuwenhoek, 105: 15–21. https://doi.org/10.1007/s10482-013-0048-5.CrossRefGoogle Scholar
Martinez-Sañudo, I., Simonato, M., Squartini, A., Mori, N., Marri, L., and Mazzon, L. 2017. Metagenomic analysis reveals changes of the Drosophila suzukii microbiota in the newly colonised regions. Insect Science, 25: 833–846. https://doi.org/10.1111/1744-7917.12458.CrossRefGoogle Scholar
Milan, N.F., Kacsoh, B.Z., and Schlenke, T.A. 2012. Alcohol consumption as self-medication against blood-borne parasites in the fruit fly. Current Biology, 22: 488–493.10.1016/j.cub.2012.01.045CrossRefGoogle ScholarPubMed
Mitsui, H., Takahashi, H.K., and Kimura, M.T. 2006. Spatial distributions and clutch sizes of Drosophila species ovipositing on cherry fruits of different stages. Population Ecology, 48: 233–237. https://doi.org/10.1007/s10144-006-0260-5.CrossRefGoogle Scholar
Morel, M.A., Ubalde, M.C., Braña, V., and Castro-Sowinski, S. 2011. Delftia sp. JD2: a potential Cr(VI)-reducing agent with plant growth-promoting activity. Archives of Microbiology, 193: 63–68. https://doi.org/10.1007/s00203-010-0632-2.CrossRefGoogle ScholarPubMed
Newell, P.D. and Douglas, A.E. 2014. Interspecies interactions determine the impact of the gut microbiota on nutrient allocation in Drosophila melanogaster . Applied & Environmental Microbiology, 80: 788–796. https://doi.org/10.1128/AEM.02742-13.CrossRefGoogle ScholarPubMed
Parshad, R. and Paika, I.J. 1964. Drosophilid survey of India II. Taxonomy and cytology of the subgenus Sophophora (Drosophila). Research Bulletin Panjab University Science, 15: 225–252.Google Scholar
Ren, L.M., Wang, L., Yu, Y., and Chu, D. 2014. Comparison of the morphological characteristics of Drosophila suzukii and other fruit flies in fruit-producing areas in China. Journal of Biosafety, 23: 178–184.Google Scholar
Ridley, E.V., Wong, A.C., Westmiller, S., and Douglas, A.E. 2012. Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster . PLOS One, 7: e36765. https://doi.org/10.1371/journal.pone.0036765.CrossRefGoogle ScholarPubMed
Rombaut, A., Guilhot, R., Xuéreb, A., Benoit, L., Chapuis, M.P., Gibert, P., and Fellous, S. 2017. Invasive Drosophila suzukii facilitates Drosophila melanogaster infestation and sour rot outbreaks in the vineyards. Royal Society Open Science, 4: 170117. https://doi.org/10.1098/rsos.170117.CrossRefGoogle ScholarPubMed
Savage, D.C. 1977. Microbial ecology of the gastrointestinal tract. Annual Reviews in Microbiology, 31: 107–133. https://doi.org/10.1146/annurev.mi.31.100177.000543.CrossRefGoogle ScholarPubMed
Schetelig, M.F., Lee, K.Z., Otto, S., Talmann, L., Stökl, J., and Degenkolb, T. 2018. Environmentally sustainable pest control options for Drosophila suzukii . Journal of Applied Entomology, 142: 3–17. https://doi.org/10.1111/jen.12469.CrossRefGoogle Scholar
Sharon, G., Segal, D., Ringo, J.M., Hefetz, A., Zilber-Rosenberg, I., and Rosenberg, E. 2010. Commensal bacteria play a role in mating preference of Drosophila melanogaster . Proceedings of the National Academy of Sciences, 107: 20051–20056. https://doi.org/10.1073/pnas.1009906107.CrossRefGoogle ScholarPubMed
Shin, S.C., Kim, S.H., You, H., Kim, B., Kim, A.C., and Lee, K.A. 2011. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science, 334: 670–674. https://doi.org/10.1126/science.1212782.CrossRefGoogle ScholarPubMed
Staubach, F., Baines, J.F., Kunzel, S., Bik, E.M., and Petrov, D.A. 2013. Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment. PLOS One, 8: e70749. https://doi.org/10.1371/journal.pone.0070749.CrossRefGoogle ScholarPubMed
Thomas, F., Hehemann, J.H., Rebuffet, E., Czjzek, M., and Michel, G. 2011. Environmental and gut bacteroidetes: the food connection. Frontiers in Microbiology, 2: 93. https://doi.org/10.3389/fmicb.2011.00093.CrossRefGoogle ScholarPubMed
Ubalde, M.C., Braña, V., Sueiro, F., and Morel, M.A. 2012. The versatility of Delftia sp. isolates as tools for bioremediation and biofertilisation technologies. Current Microbiology, 64: 597–603. https://doi.org/10.1007/s00284-012-0108-5.CrossRefGoogle Scholar
Wang, H.D., Shen, Y., Wang, E.G., Huang, Q.B., and Xu, Z.H. 2017. Monitoring and integrated control of population dynamics of bat fly on red bayberry. Journal of Agriculture, 7: 6–14.Google Scholar
Warnecke, F., Luginbühl, P., Ivanova, N., Ghassemian, M., Richardson, T.H., and Stege, J.T. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature, 450: 560–565. https://doi.org/ 10.1038/nature06269.CrossRefGoogle ScholarPubMed
Winans, N.J., Walter, A., Chouaia, B., Chaston, G.M., Douglas, A.E., and Newell, P.D. 2017. A genomic investigation of ecological differentiation between free-living and Drosophila-associated bacteria. Molecular Ecology, 26: 4536–4550. https://doi.org/ 10.1111/mec.14232.CrossRefGoogle ScholarPubMed
Wong, A.C., Dobson, A.J., and Douglas, A.E. 2014. Gut microbiota dictates the metabolic response of Drosophila to diet. Journal of Experimental Biology, 217: 1894–1901. https://doi.org/10.1242/jeb.101725.Google Scholar
Yun, J.H., Roh, S.W., Whon, T.W., Jung, M.J., Kim, M.S., and Park, D.S. 2014. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Applied and Environmental Microbiology, 80: 5254–5264. https://doi.org/10.1128/AEM.01226-14.CrossRefGoogle ScholarPubMed
Zhai, Y., Lin, Q.C., Zhang, J., Zhang, F., Zheng, L., and Yu, Y. 2016. Adult reproductive diapause in Drosophila suzukii females. Journal of Pest Science, 89: 679–688. https://doi.org/10.1007/s10340-016-0760-9.CrossRefGoogle Scholar
Zhai, Y.F., Yu, Y., Lin, Q.C., Zhou, X.H., Li, L.L., Zhuang, Q.Y., et al. 2014. An artificial diet for Drosophila suzukii. State Intellectual Property Office of the People’s Republic of China. 201410162636.6.Google Scholar
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