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Persistence of diet effects on the microbiota of Drosophila suzukii (Diptera: Drosophilidae)

Published online by Cambridge University Press:  22 June 2020

Yanira Jiménez-Padilla ,
Ebenezer O. Esan ,
Kevin D. Floate Open the ORCID record for Kevin D. Floate [Opens in a new window]  and
Brent J. Sinclair Open the ORCID record for Brent J. Sinclair [Opens in a new window]
Yanira Jiménez-Padilla
Affiliation:
1Department of Biology, University of Western Ontario, London, Ontario, N6A 5B7, Canada
Ebenezer O. Esan
Affiliation:
1Department of Biology, University of Western Ontario, London, Ontario, N6A 5B7, Canada
Kevin D. Floate
Affiliation:
2Lethbridge Research and Development Centre, Agriculture and Agri-food Canada, Alberta, T1J 4B1, Canada
Brent J. Sinclair*
Affiliation:
1Department of Biology, University of Western Ontario, London, Ontario, N6A 5B7, Canada
*
*Corresponding author: Email: bsincla7@uwo.ca
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Abstract

The insect commensal microbiota consists of prokaryotes and eukaryotes. We explored the effect of diet and the persistence of the gut microbiota across generations in Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). We transferred subsets of a single population of D. suzukii to different fruit-based diets (blueberry (Vaccinium Linnaeus; Ericaceae), raspberry (Rubus Linnaeus; Rosaceae), and strawberry (Fragaria × ananassa Duchesne; Rosaceae)) for three generations and then returned them to a common, banana-based, diet. We used 16S rDNA (Bacteria) and ITS (internal transcribed spacer; Fungi) sequencing of female endosymbiont-free flies to identify the microbiota. We identified 2700 bacterial and 350 fungal operational taxonomic units (OTUs); there was no correlation between the number of bacterial and fungal OTUs in a sample. Bacterial communities were dominated by Proteobacteria (especially Acetobacteraceae); Ascomycota dominated the fungal communities. Species diversity of both bacteria and fungi differed among diets, but there were no differences in species-level diversity when these D. suzukii were returned to a control diet. A principle coordinates analysis revealed no differences in the bacterial or fungal community in the first generation on fruit diets, but that the communities diverged over the next two generations; neither fungal and bacterial communities converged after one generation on control food. We conclude that diet changes the D. suzukii microbiota, and that these changes persist for more than one generation.

Type
Research Papers
Information
The Canadian Entomologist , Volume 152 , Issue 4: The spotted-wing drosophila , August 2020 , pp. 516 - 531
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Copyright
© Crown Copyright and The Author(s), 2020. Published by Cambridge University Press on behalf of the Entomological Society of Canada

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Footnotes

Subject editor: Suzanne Blatt

References

Adair, K.L. and Douglas, A.E. 2017. Making a microbiome: the many determinants of host-associated microbial community composition. Current Opinion in Microbiology, 35: 23–29.CrossRefGoogle ScholarPubMed
Adair, K.L., Wilson, M., Bost, A., and Douglas, A.E. 2018. Microbial community assembly in wild populations of the fruit fly Drosophila melanogaster. ISME Journal, 12: 959–972.CrossRefGoogle ScholarPubMed
Anagnostou, C., Dorsch, M., and Rohlfs, M. 2010. Influence of dietary yeasts on Drosophila melanogaster life-history traits. Entomologia Experimentalis et Applicata, 136: 1–11.CrossRefGoogle Scholar
Asplen, M.K., Anfora, G., Biondi, A., Choi, D.S., Chu, D., Daane, K.M., et al. 2015. Invasion biology of spotted wing drosophila (Drosophila suzukii): a global perspective and future priorities. Journal of Pest Science, 88: 469–494.CrossRefGoogle Scholar
Bahrndorff, S., Alemu, T., Alemneh, T., and Nielsen, J.L. 2016. The microbiome of animals: implications for conservation biology. International Journal of Genomics, 2016: 5304028.CrossRefGoogle ScholarPubMed
Bakula, M. 1969. Persistence of a microbial flora during postembryogenesis of Drosophila melanogaster. Journal of Invertebrate Pathology, 14: 365–374.CrossRefGoogle ScholarPubMed
Bing, X., Gerlach, J., Loeb, G., and Buchon, N. 2018. Nutrient-dependent impact of microbes on Drosophila suzukii development. mBio, 9: e02199–02117.Google Scholar
Blum, J.E., Fischer, C.N., Miles, J., and Handelsman, J. 2013. Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster. mBio, 4: e00860–00813.Google Scholar
Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., and Holmes, S.P. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods, 13: 581–583.CrossRefGoogle ScholarPubMed
Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Lozupone, C.A., Turnbaugh, P.J., et al. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America, 108: 4516–4522.Google Scholar
Chandler, J.A., Eisen, J.A., and Kopp, A. 2012. Yeast communities of diverse Drosophila species: comparison of two symbiont groups in the same hosts. Applied and Environmental Microbiology, 78: 7327–7336.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. PeerJ, 2: 10.CrossRefGoogle ScholarPubMed
Chandler, J.A., Liu, R.M., and Bennett, S.N. 2015. RNA shotgun metagenomic sequencing of northern California (USA) mosquitoes uncovers viruses, bacteria, and fungi. Frontiers in Microbiology, 6: 16.CrossRefGoogle ScholarPubMed
Chandler, J.A., Morgan Lang, 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.CrossRefGoogle ScholarPubMed
Chong, J., Liu, P., Zhou, G., and Xia, J. 2020. Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nature Protocols, 15: 799–821.CrossRefGoogle ScholarPubMed
Colinet, H. and Renault, D. 2014. Dietary live yeast alters metabolic profiles, protein biosynthesis and thermal stress tolerance of Drosophila melanogaster. Comparative Biochemistry and Physiology A, 170: 6–14.CrossRefGoogle ScholarPubMed
Dhariwal, A., Chong, J., Habib, S., King, I.L., Agellon, L.B., and Xia, J.G. 2017. MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Research, 45: W180–W188.CrossRefGoogle ScholarPubMed
Douglas, A.E. 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annual Review of Entomology, 60: 17–34.CrossRefGoogle ScholarPubMed
Douglas, A.E. 2018a. The Drosophila model for microbiome research. Lab Animal, 47: 157–164.CrossRefGoogle ScholarPubMed
Douglas, A.E. 2018b. Fundamentals of microbiome science. Princeton University Press, Princeton, New Jersey, United States of America.Google Scholar
Ebbert, M.A., Marlowe, J.L., and Burkholder, J.J. 2003. Protozoan and intracellular fungal gut endosymbionts in Drosophila: prevalence and fitness effects of single and dual infections. Journal of Invertebrate Pathology, 83: 37–45.CrossRefGoogle ScholarPubMed
Ferguson, L.V., Dhakal, P., Lebenzon, J.E., Heinrichs, D.E., Bucking, C., and Sinclair, B.J. 2018. Seasonal shifts in the insect gut microbiome are concurrent with changes in cold tolerance and immunity. Functional Ecology, 32: 2357–2368.CrossRefGoogle Scholar
Fountain, M.T., Bennett, J., Cobo-Medina, M., Conde Ruiz, R., Deakin, G., and Delgado, A., et al. 2018. Alimentary microbes of winter-form Drosophila suzukii. Insect Molecular Biology, 27: 383–392.CrossRefGoogle ScholarPubMed
Fricker, A.M., Podlesny, D., and Fricke, W.F. 2019. What is new and relevant for sequencing-based microbiome research? A mini-review. Journal of Advanced Research, 19: 105–112.CrossRefGoogle ScholarPubMed
Fromont, C., Adair, K.L., and Douglas, A.E. 2019. Correlation and causation between the microbiome, Wolbachia and host functional traits in natural populations of drosophilid flies. Molecular Ecology, 28: 1826–1841.CrossRefGoogle ScholarPubMed
Hamby, K.A., Hernandez, A., Boundy-Mills, K., and Zalom, F.G. 2012. Associations of yeasts with spotted-wing drosophila (Drosophila suzukii; Diptera: Drosophilidae) in cherries and raspberries. Applied and Environmental Microbiology, 78: 4869–4873.CrossRefGoogle ScholarPubMed
Henry, L.M., Maiden, M.C., Ferrari, J., and Godfray, H.C. 2015. Insect life history and the evolution of bacterial mutualism. Ecology Letters, 18: 516–525.CrossRefGoogle ScholarPubMed
Hill, J.E., Seipp, R.P., Betts, M., Hawkins, L., Van Kessel, A.G., Crosby, W.L., and Hemmingsen, S.M. 2002. Extensive profiling of a complex microbial community by high-throughput sequencing. Applied and Environmental Microbiology, 68: 3055–3066.CrossRefGoogle ScholarPubMed
Hosokawa, T., Koga, R., Kikuchi, Y., Meng, X.Y., and Fukatsu, T. 2010. As a bacteriocyte-associated nutritional mutualist. Proceedings of the National Academy of Sciences of the United States of America, 107: 769–774.Google Scholar
Huang, J.H., Jing, X., and Douglas, A.E. 2015. The multi-tasking gut epithelium of insects. Insect Biochemistry and Molecular Biology, 67: 15–20.CrossRefGoogle ScholarPubMed
Jakobs, R., Gariepy, T.D., and Sinclair, B.J. 2015. Adult plasticity of cold tolerance in a continental-temperate population of Drosophila suzukii. Journal of Insect Physiology, 79: 1–9.CrossRefGoogle Scholar
Jaramillo, S.L., Mehlferber, E., and Moore, P.J. 2015. Life-history trade-offs under different larval diets in Drosophila suzukii (Diptera: Drosophilidae). Physiological Entomology, 40: 2–9.CrossRefGoogle Scholar
Jehrke, L., Stewart, F.A., Droste, A., and Beller, M. 2018. The impact of genome variation and diet on the metabolic phenotype and microbiome composition of Drosophila melanogaster. Scientific Reports, 8: 15.CrossRefGoogle ScholarPubMed
Jiménez Padilla, Y. 2016. Effects of gut-associated yeasts on Drosophila melanogaster performance. M.Sc. thesis. University of Western Ontario, London, Ontario, Canada. Available from https://ir.lib.uwo.ca/etd/4285 [accessed 3 May 2020].Google Scholar
Jiménez Padilla, Y., Ferguson, L.V., and Sinclair, B.J. 2020. Comparing apples and oranges (and blueberries and grapes): fruit type affects development and cold-susceptibility of immature Drosophila suzukii (Dipetera: Drosophilidae). The Canadian Entomologist, this issue.CrossRefGoogle Scholar
Koga, R., Meng, X.Y., Tsuchida, T., and Fukatsu, T. 2012. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. Proceedings of the National Academy of Sciences of the United States of America, 109: E1230–E1237.Google Scholar
Lachance, M.A., Gilbert, D.G., and Starmer, W.T. 1995. Yeast communities associated with Drosophila species and related flies in an eastern oak-pine forest: a comparison with western communities. Journal of Industrial Microbiology, 14: 484–494.CrossRefGoogle Scholar
Lewis, M.T. and Hamby, K.A. 2019. Differential impacts of yeasts on feeding behavior and development in larval Drosophila suzukii (Diptera: Drosophilidae). Scientific Reports, 9: 12.CrossRefGoogle Scholar
Li, Y.Y., Fields, P.G., Pang, B.P., Coghlin, P.C., and Floate, K.D. 2015. Prevalence and diversity of Wolbachia bacteria infecting insect pests of stored products. Journal of Stored Products Research, 62: 93–100.CrossRefGoogle Scholar
Markow, T.A. and O’Grady, P. 2005. Drosophila: a guide to species identification and use. Academic Press, London, United Kingdom.CrossRefGoogle Scholar
Martin, K.J. and Rygiewicz, P.T. 2005. Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiology, 5: 28–28.CrossRefGoogle ScholarPubMed
Martinez-Sañudo, I., Simonato, M., Squartini, A., Mori, N., Marri, L., and Mazzon, L. 2018. Metagenomic analysis reveals changes of the Drosophila suzukii microbiota in the newly colonized regions: microbiota associated to Drosophila suzukii. Insect Science, 25: 833–846.CrossRefGoogle Scholar
McFall-Ngai, M., Hadfield, M.G., Bosch, T.C., Carey, H.V., Domazet-Loso, T., Douglas, A.E., et al. 2013. Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences of the United States of America, 110: 3229–3236.Google Scholar
Pais, I.S., Valente, R.S., Sporniak, M., and Teixeira, L. 2018. Drosophila melanogaster establishes a species-specific mutualistic interaction with stable gut-colonizing bacteria. PLoS Biology, 16: 45.CrossRefGoogle ScholarPubMed
Phaff, H.J., Miller, M.W., and Shifrine, M. 1956. The taxonomy of yeasts isolated from Drosophila in the Yosemite region of California. Antonie van Leeuwenhoek, 22: 145–161.CrossRefGoogle ScholarPubMed
Rahman, N.A., Parks, D.H., Willner, D.L., Engelbrektson, A.L., Goffredi, S.K., Warnecke, F., et al. 2015. A molecular survey of Australian and North American termite genera indicates that vertical inheritance is the primary force shaping termite gut microbiomes. Microbiome, 3: 16.Google ScholarPubMed
Ren, C., Webster, P., Finkel, S.E., and Tower, J. 2007. Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metabolism, 6: 144–152.CrossRefGoogle ScholarPubMed
Rota-Stabelli, O., Blaxter, M., and Anfora, G. 2013. Drosophila suzukii. Current Biology, 23: R8–R9.CrossRefGoogle ScholarPubMed
Shin, S.C., Kim, S.H., You, H., Kim, B., Kim, A.C., Lee, K.A., et al. 2011. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science, 334: 670–674.CrossRefGoogle ScholarPubMed
Solomon, G.M., Dodangoda, H., McCarthy-Walker, T., Ntim-Gyakari, R., and Newell, P.D. 2019. The microbiota of Drosophila suzukii influences the larval development of Drosophila melanogaster. PeerJ, 7: 24.CrossRefGoogle ScholarPubMed
Starmer, W.T. and Fogleman, J.C. 1986. Coadaptation of Drosophila and yeasts in their natural habitat. Journal of Chemical Ecology, 12: 1037–1055.CrossRefGoogle Scholar
Storelli, G., Defaye, A., Erkosar, B., Hols, P., Royet, J., and Leulier, F. 2011. Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metabolism, 14: 403–414.CrossRefGoogle ScholarPubMed
Videira, S.I.R., Groenewald, J.Z., Nakashima, C., Braun, U., Barreto, R.W., de Wit, P., and Crous, P.W. 2017. Mycosphaerellaceae - chaos or clarity?. Studies in Mycology, 87: 257–421.CrossRefGoogle ScholarPubMed
Wang, X.W., Yang, F.Y., Meijer, M., Kraak, B., Sun, B.D., Jiang, Y.L., et al. 2019. Redefining Humicola sensu stricto and related genera in the Chaetomiaceae. Studies in Mycology, 93: 65–153.CrossRefGoogle ScholarPubMed
Wong, A.C.N., Chaston, J.M., and Douglas, A.E. 2013. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. International Society for Microbial Ecology Journal, 7: 1922–1932.Google ScholarPubMed
Wong, A.C.N., 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.CrossRefGoogle Scholar
Wong, A.C.N., Luo, Y., Jing, X., Franzenburg, S., Bost, A., and Douglas, A.E. 2015. The host as the driver of the microbiota in the gut and external environment of Drosophila melanogaster. Applied and Environmental Microbiology, 81: 6232–6240.CrossRefGoogle ScholarPubMed
Wong, A.C.N., Ng, P., and Douglas, A.E. 2011. Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environmental Microbiology, 13: 1889–1900.CrossRefGoogle ScholarPubMed
Wu, G.D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y.Y., Keilbaugh, S.A., et al. 2011. Linking long-term dietary patterns with gut microbial enterotypes. Science, 334: 105–108.CrossRefGoogle ScholarPubMed
Zhang, N., Suh, S.O., and Blackwell, M. 2003. Microorganisms in the gut of beetles: evidence from molecular cloning. Journal of Invertebrate Pathology, 84: 226–233.CrossRefGoogle ScholarPubMed
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