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The Drosophila model for microbiome research

Lab Animal volume 47, pages 157–164 (2018)Cite this article

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Abstract

The gut microbiome is increasingly recognized to play an important role in shaping the health and fitness of animals, including humans. Drosophila is emerging as a valuable model for microbiome research, combining genetic and genomic resources with simple protocols to manipulate the microbiome, such that microbiologically sterile flies and flies bearing a standardized microbiota can readily be produced in large numbers. Studying Drosophila has the potential to increase our understanding of how the microbiome influences host traits, and allows opportunities for hypothesis testing of microbial impacts on human health. Drosophila is being used to investigate aspects of host-microbe interactions, including the metabolism, the immune system and behavior. Drosophila offers a valuable alternative to rodent and other mammalian models of microbiome research for fundamental discovery of microbiome function, enabling improved research cost effectiveness and benefits for animal welfare.

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Fig. 1: The Drosophila gut microbiome is amenable to manipulation, to generate axenic flies (i.e. microbiologically sterile, often referred to as “germ-free”) and gnotobiotic flies (i.e. with a standardized microbiota).
Fig. 2: The organization of the Drosophila gut.
Fig. 3: Contribution of the gut microbiota to Drosophila nutrition.

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References

  1. Letsou, A. & Bohmann, D. Small flies–big discoveries: nearly a century of Drosophila genetics and development. Dev. Dyn. 232, 526–528 (2005).

    Article  PubMed  CAS  Google Scholar 

  2. Broderick, N. A. & Lemaitre, B. Gut-associated microbes of Drosophila melanogaster. Gut microbes 3, 307–321 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Ren, C., Webster, P., Finkel, S. E. & Tower, J. Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metab. 6, 144–52 (2007).

    Article  PubMed  CAS  Google Scholar 

  4. Clark, M. E., Anderson, C. L., Cande, J. & Karr, T. L. Widespread prevalence of Wolbachia in laboratory stocks and the implications for Drosophila research. Genetics 170, 1667–1675 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Riegler, M., Sidhu, M., Miller, W. J. & O’Neill, S. L. Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr. Biol. 15, 1428–1433 (2005).

    Article  PubMed  CAS  Google Scholar 

  6. Haselkorn, T. S., Markow, T. A. & Moran, N. A. Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol. Ecol. 18, 1294–1305 (2009).

    Article  PubMed  CAS  Google Scholar 

  7. Beckmann, J. F., Ronau, J. A. & Hochstrasser, M. A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat. Microbiol. 2, 17007 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Paredes, J. C., Herren, J. K., Schupfer, F. & Lemaitre, B. The role of lipid competition for endosymbiont-mediated protection against parasitoid wasps in Drosophila. mBio 7 (2016).

  9. Teixeira, L., Ferreira, A. & Ashburner, M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 6, e2 (2008).

    Article  PubMed  CAS  Google Scholar 

  10. Hedges, L. M., Brownlie, J. C., O’Neill, S. L. & Johnson, K. N. Wolbachia and virus protection in insects. Science 322, 702 (2008).

    Article  PubMed  CAS  Google Scholar 

  11. Serbus, L. R., Casper-Lindley, C., Landmann, F. & Sullivan, W. The genetics and cell biology of Wolbachia-host interactions. Annu. Rev. Genet. 42, 683–707 (2008).

    Article  PubMed  CAS  Google Scholar 

  12. Werren, J. H., Baldo, L. & Clark, M. E. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6, 741–751 (2008).

    Article  PubMed  CAS  Google Scholar 

  13. Anbutsu, H. & Fukatsu, T. Spiroplasma as a model insect endosymbiont. Environ. Microbiol. Rep. 3, 144–153 (2011).

    Article  PubMed  CAS  Google Scholar 

  14. Haselkorn, T. S. The Spiroplasma heritable bacterial endosymbiont of Drosophila. Fly (Austin) 4, 80–87 (2010).

    Article  CAS  Google Scholar 

  15. Koyle, M. L. et al. Rearing the fruit fly Drosophila melanogaster under axenic and gnotobiotic conditions. J. Vis. Exp. 113, e54219 (2016).

    Google Scholar 

  16. Trinder, M., Daisley, B. A., Dube, J. S. & Reid, G. Drosophila melanogaster as a high-throughput model for host-microbiota interactions. Front Microbiol. 8, 751 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Brummel, T. et al. Drosophila lifespan enhancement by exogenous bacteria. Proc. Natl Acad. Sci. U S A 101, 12974–9 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Erkosar, B., Storelli, G., Defaye, A. & Leulier, F. Host-intestinal microbiota mutualism: “learning on the fly”. Cell Host Microbe 13, 8–14 (2013).

    Article  PubMed  CAS  Google Scholar 

  19. Newell, P. D. & Douglas, A. E. Interspecies interactions determine the impact of the gut microbiota on nutrient allocation in Drosophila melanogaster. Appl. Environ. Microbiol. 80, 788–796 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Broderick, N. A., Buchon, N. & Lemaitre, B. Microbiota-induced changes in Drosophila melanogaster host gene expression and gut morphology. mBio 5, e01117–14 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Simpson, S. J. & Douglas, A. E. The Insects: Structure and Function. Edn. 5th., (Cambridge University Press, Cambridge, UK, 2012).

    Google Scholar 

  22. Lemaitre, B. & Miguel-Aliaga, I. The digestive tract of Drosophila melanogaster. Annu. Rev. Genetics 47, 377–404 (2013).

    Article  CAS  Google Scholar 

  23. Buchon, N., Broderick, N. A. & Lemaitre, B. Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat. Rev. Microbiol. 11, 615–626 (2013).

    Article  PubMed  CAS  Google Scholar 

  24. Izumi, Y., Motoishi, M., Furuse, K. & Furuse, M. A tetraspanin regulates septate junction formation in Drosophila midgut. J Cell Sci. 129, 1155–1164 (2016).

    Article  PubMed  CAS  Google Scholar 

  25. Limmer, S., Weiler, A., Volkenhoff, A., Babatz, F. & Klambt, C. The Drosophila blood-brain barrier: development and function of a glial endothelium. Front Neurosci. 8, 365 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  26. King, D. G. Cellular organization and peritrophic membrane formation in the cardia (proventriculus) of Drosophila melanogaster. J. Morphol. 196, 253–282 (1988).

  27. Lang, T. et al. Searching the evolutionary origin of epithelial mucus protein components-mucins and FCGBP. Mol. Biol. Evol. 33, 1921–1936 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Tailford, L. E. et al. Discovery of intramolecular trans-sialidases in human gut microbiota suggests novel mechanisms of mucosal adaptation. Nat. Commun. 6, 7624 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kuraishi, T., Binggeli, O., Opota, O., Buchon, N. & Lemaitre, B. Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 108, 15966–15971 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Rodgers, F. H., Gendrin, M., Wyer, C. A. S. & Christophides, G. K. Microbiota-induced peritrophic matrix regulates midgut homeostasis and prevents systemic infection of malaria vector mosquitoes. PLoS Pathog. 13, e1006391 (2017).

  31. Shanbhag, S. & Tripathi, S. Epithelial ultrastructure and cellular mechanisms of acid and base transport in the Drosophila midgut. J. Exp. Biol. 212, 1731–1744 (2009).

    Article  PubMed  CAS  Google Scholar 

  32. Lin, W.-S. et al. Reduced gut acidity induces an obese-like phenotype in Drosophila melanogaster and in mice. PLoS One 10, e0139722 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Overend, G. et al. Molecular mechanism and functional significance of acid generation in the Drosophila midgut. Sci. Rep. 6, 27242 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Li, H., Qi, Y. & Jasper, H. Preventing age-related decline of gut compartmentalization limits microbiota dysbiosis and extends lifespan. Cell Host Microbe 19, 240–253 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Broderick, N.A. Friend, foe or food? Recognition and the role of antimicrobial peptides in gut immunity and Drosophila-microbe interactions. Philos Trans. R Soc. Lond. B Biol. Sci. 371 (2016).

  36. Ryu, J. H. et al. Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319, 777–782 (2008).

    Article  PubMed  CAS  Google Scholar 

  37. Ha, E. M., Oh, C. T., Bae, Y. S. & Lee, W. J. A direct role for dual oxidase in Drosophila gut immunity. Science 310, 847–850 (2005).

    Article  PubMed  CAS  Google Scholar 

  38. Lee, K. A. et al. Bacterial uracil modulates Drosophila DUOX-dependent gut immunity via Hedgehog-induced signaling endosomes. Cell Host Microbe 17, 191–204 (2015).

    Article  PubMed  CAS  Google Scholar 

  39. Lee, K. A. et al. Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell 153, 797–811 (2013).

    Article  PubMed  CAS  Google Scholar 

  40. Obadia, B. et al. Probabilistic invasion underlies natural gut microbiome stability. Curr. Biol. 27, 1999–2006.e8 (2017).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  41. Chaston, J. M., Newell, P. D. & Douglas, A. E. Metagenome-wide association of microbial determinants of host phenotype in Drosophila melanogaster. mBio 5, e01631–01614 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Shin, S. C. et al. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334, 670–674 (2011).

    Article  PubMed  CAS  Google Scholar 

  43. Huang, J. H. & Douglas, A. E. Consumption of dietary sugar by gut bacteria determines Drosophila lipid content. Biol. Lett. 11, 20150469 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Wong, A. C., Chaston, J. M. & Douglas, A. E. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J. 7, 1922–1932 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Chandler, J. A., Lang, J. M., Bhatnagar, S., Eisen, J. A. & Kopp, A. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLoS Genet. 7, e1002272 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Wong, C. N., Ng, P. & Douglas, A. E. Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environ. Microbiol. 13, 1889–1900 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Blum, J. E., Fischer, C. N., Miles, J. & Handelsman, J. Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster. mBio 4, e00860–00813 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Fink, C., Staubach, F., Kuenzel, S., Baines, J. F. & Roeder, T. Noninvasive analysis of microbiome dynamics in the fruit fly Drosophila melanogaster. Appl. Environ. Microbiol. 79, 6984–6988 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Sebald, J. et al. Impact of the chromatin remodeling factor CHD1 on gut microbiome composition of Drosophila melanogaster. PLoS One 11, e0153476 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Chaston, J. M., Dobson, A. J., Newell, P. D. & Douglas, A. E. Host genetic control of the microbiota mediates the Drosophila nutritional phenotype. Appl. Environ. Microbiol. 82, 671–679 (2015).

    Article  PubMed  CAS  Google Scholar 

  51. Cox, C. R. & Gilmore, M. S. Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infec. Immun. 75, 1565–1567 (2007).

    Article  CAS  Google Scholar 

  52. Bost, A. et al. How gut transcriptional function of Drosophila melanogaster varies with the presence and composition of the gut microbiota. Mol. Ecol. (2017). Epub 7 Nov.

  53. Staubach, F., Baines, J. F., Kunzel, S., Bik, E. M. & Petrov, D. A. Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment. PLoS One 8, e70749 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Corby-Harris, V. et al. Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster. Appl. Environ. Microbiol. 73, 3470–3479 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Adair, K.L., Wilson, M., Bost, A. & Douglas, A.E. Microbial community assembly in wild populations of the fruit fly Drosophila melanogaster. ISME J. Epub 22 Jan (2018).

  56. Winans, N. J. et al. A genomic investigation of ecological differentiation between free-living and Drosophila-associated bacteria. Mol. Ecol. 26, 4536–4550 (2017).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  57. Chandler, J. A., Eisen, J. A. & Kopp, A. Yeast communities of diverse Drosophila species: comparison of two symbiont groups in the same hosts. Appl. Environ. Microbiol. 78, 7327–7336 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Stamps, J. A., Yang, L. H., Morales, V. M. & Boundy-Mills, K. L. Drosophila regulate yeast density and increase yeast community similarity in a natural substrate. PLoS One 7, e42238 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Lam, S. S. & Howell, K. S. Drosophila-associated yeast species in vineyard ecosystems. FEMS Microbiol. Lett. 362 (2015).

  60. Hoang, D., Kopp, A. & Chandler, J. A. Interactions between Drosophila and its natural yeast symbionts - Is Saccharomyces cerevisiae a good model for studying the fly-yeast relationship? PeerJ. 3, e1116 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Inamine, H. et al. Spatiotemporally heterogeneous population dynamics of gut bacteria inferred from fecal time series data. mBio 9, e01453–17 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Storelli, G. et al. Drosophila perpetuates nutritional mutualism by promoting the fitness of its intestinal symbiont Lactobacillus plantarum. Cell Metab. 27, 362–377 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Wong, A. C. et al. The host as the driver of the microbiota in the gut and external environment of Drosophila melanogaster. Appl. Environ. Microbiol. 81, 6232–6240 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Franklin, C. L. & Ericsson, A. C. Microbiota and reproducibility of rodent models. Lab Anim. (NY) 46, 114–122 (2017).

    Article  Google Scholar 

  65. McCafferty, J. et al. Stochastic changes over time and not founder effects drive cage effects in microbial community assembly in a mouse model. ISME J. 7, 2116–2125 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Campbell, J. H. et al. Host genetic and environmental effects on mouse intestinal microbiota. ISME J. 6, 2033–2044 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Ridley, E. V., Wong, A. C. & Douglas, A. E. Microbe-dependent and nonspecific effects of procedures to eliminate the resident microbiota from Drosophila melanogaster. Appl. Environ. Microbiol. 79, 3209–3214 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Bakula, M. The persistence of a microbial flora during postembryogenesis of Drosophila melanogaster. J. Invertebr. Pathol. 14, 365–374 (1969).

    Article  PubMed  CAS  Google Scholar 

  69. Ballard, J. W. & Melvin, R. G. Tetracycline treatment influences mitochondrial metabolism and mtDNA density two generations after treatment in Drosophila. Insect. Mol. Biol. 16, 799–802 (2007).

    Article  PubMed  CAS  Google Scholar 

  70. Ridley, E. V., Wong, A. C., Westmiller, S. & Douglas, A. E. Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster. PLoS One 7, e36765 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Storelli, G. et al. Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab. 14, 403–414 (2011).

    Article  PubMed  CAS  Google Scholar 

  72. Sang, J. H. The quantitative nutritional requirements of Drosophila melanogaster. J. Exp. Biol. 33, 45–72 (1956).

    CAS  Google Scholar 

  73. Douglas, A. E. The B vitamin nutrition of insects: the contributions of diet, microbiome and horizontally-acquired genes. Curr. Opin. Insect. Sci. 23, 65–69 (2017).

    Article  PubMed  Google Scholar 

  74. Wong, A. C., Dobson, A. J. & Douglas, A. E. Gut microbiota dictates the metabolic response of Drosophila to diet. J. Exp. Biol. 217, 1894–1901 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  75. Piper, M. D. et al. A holidic medium for Drosophila melanogaster. Nat. Methods 11, 100–105 (2014).

    Article  PubMed  CAS  Google Scholar 

  76. Thompson, S. N. The insect ‘blood’ sugar. Adv. Insect. Physiol. 31, 205–285 (2003).

    Article  CAS  Google Scholar 

  77. Smith, K., McCoy, K. D. & Macpherson, A. J. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Sem. Immunol. 19, 59–69 (2007).

    Article  CAS  Google Scholar 

  78. Fischer, C. N. et al. Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior. eLife 6 (2017).

  79. Kim, G., Huang, J. H., McMullen, J. G., 2nd, Newell, P. D. & Douglas, A. E. Physiological responses of insects to microbial fermentation products: Insights from the interactions between Drosophila and acetic acid. J. Insect. Physiol. Epub 15 May (2017).

  80. Cox, L. M. & Blaser, M. J. Antibiotics in early life and obesity. Nat. Rev. Endocrinol. 11, 182–190 (2015).

    Article  PubMed  Google Scholar 

  81. Zoetendal, E. G. et al. The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J. 6, 1415–1426 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Fushimi, T. & Sato, Y. Effect of acetic acid feeding on the circadian changes in glycogen and metabolites of glucose and lipid in liver and skeletal muscle of rats. Br. J. Nutr. 94, 714–719 (2005).

    Article  PubMed  CAS  Google Scholar 

  83. Yamada, R., Deshpande, S. A., Bruce, K. D., Mak, E. M. & Ja, W. W. Microbes promote amino acid harvest to rescue undernutrition in Drosophila. Cell Rep. 10, 865–872 (2015).

    Article  CAS  Google Scholar 

  84. Leitao-Goncalves, R. et al. Commensal bacteria and essential amino acids control food choice behavior and reproduction. PLoS Biol. 15, e2000862 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Behmer, S. T. & Nes, W. D. Insect sterol nutrition and physiology: a global overview. Adv. Insect. Physiol. 31, 1–72 (2003).

  86. Niwa, R. & Niwa, Y. S. The fruit fly Drosophila melanogaster as a model system to study cholesterol metabolism and homeostasis. Cholesterol 2011, 176802 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Elya, C., Zhang, V., Ludington, W. B. & Eisen, M. B. Stable host gene expression in the gut of adult Drosophila melanogaster with different bacterial mono-associations. PLoS One 11, e0167357 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Erkosar, B. et al. Drosophila microbiota modulates host metabolic gene expression via IMD/NF-kappaB signaling. PLoS One 9, e94729 (2014).

    Article  PubMed  CAS  Google Scholar 

  89. Dobson, A. J., Chaston, J. M. & Douglas, A. E. The Drosophila transcriptional network is structured by microbiota. BMC Genomics 17, 975 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Huang, W. et al. Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines. Genome Res. 24, 1193–1208 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Mackay, T. F. et al. The Drosophila melanogaster Genetic Reference Panel. Nature 482, 173–178 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Dobson, A. J. et al. Host genetic determinants of microbiota-dependent nutrition revealed by genome-wide analysis of Drosophila melanogaster. Nat. Commun. 6, 6312 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Goodrich, J. K., Davenport, E. R., Waters, J. L., Clark, A. G. & Ley, R. E. Cross-species comparisons of host genetic associations with the microbiome. Science 352, 532–535 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Nguyen, T. L., Vieira-Silva, S., Liston, A. & Raes, J. How informative is the mouse for human gut microbiota research? Dis. Model Mech. 8, 1–16 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Arrieta, M. C., Walter, J. & Finlay, B. B. Human microbiota-associated mice: A model with challenges. Cell Host Microbe 19, 575–578 (2016).

    Article  PubMed  CAS  Google Scholar 

  96. Guo, L., Karpac, J., Tran, S. L. & Jasper, H. PGRP-SC2 promotes gut immune homeostasis to limit commensal dysbiosis and extend lifespan. Cell 156, 109–122 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Lhocine, N. et al. PIMS modulates immune tolerance by negatively regulating Drosophila innate immune signaling. Cell Host Microbe 4, 147–158 (2008).

    Article  PubMed  CAS  Google Scholar 

  98. Rooks, M. G. & Garrett, W. S. Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol. 16, 341–352 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Round, J. L. & Mazmanian, S. K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313–323 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Benoit, J. B. et al. Symbiont-induced odorant binding proteins mediate insect host hematopoiesis. eLife 6, e19535 (2017).

  101. Sansone, C. L. et al. Microbiota-dependent priming of antiviral intestinal immunity in Drosophila. Cell Host Microbe 18, 571–581 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Thevaranjan, N. et al. Age-associated microbial dysbiosis promotes intestinal permeability, systemic inflammation, and macrophage dysfunction. Cell Host Microbe 21, 455–66 (2017).

  103. Clark, R. I. et al. Distinct shifts in microbiota composition during Drosophila aging impair intestinal function and drive mortality. Cell Rep. 12, 1656–67 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Vuong, H. E., Yano, J. M., Fung, T. C. & Hsiao, E. Y. The microbiome and host behavior. Annu. Rev. Neurosci. 40, 21–49 (2017).

    Article  PubMed  CAS  Google Scholar 

  105. Forsythe, P., Kunze, W. & Bienenstock, J. Moody microbes or fecal phrenology: what do we know about the microbiota-gut-brain axis? BMC Med. 14, 58 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  106. Wong, A. C. et al. Gut microbiota modifies olfactory-guided microbial preferences and foraging decisions in Drosophila. Curr. Biol. 27, 2397–2404 (2017). e2394.

    Article  PubMed  CAS  Google Scholar 

  107. Sharon, G. et al. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc. Natl Acad. Sci. U S A 107, 20051–20056 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  108. Najarro, M. A., Sumethasorn, M., Lamoureux, A. & Turner, T. L. Choosing mates based on the diet of your ancestors: replication of non-genetic assortative mating in Drosophila melanogaster. PeerJ 3, e1173 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  109. Leftwich, P. T., Clarke, N. V. E., Hutchings, M. I. & Chapman, T. Gut microbiomes and reproductive isolation in Drosophila. Proc. Natl Acad. Sci. USA 114, 12767–12772 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  110. Rosselot, A. E., Hong, C. I. & Moore, S. R. Rhythm and bugs: circadian clocks, gut microbiota, and enteric infections. Curr. Opin. Gastroenterol. 32, 7–11 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  111. Voigt, R. M., Forsyth, C. B., Green, S. J., Engen, P. A. & Keshavarzian, A. Circadian rhythm and the gut microbiome. Int. Rev. Neurobiol. 131, 193–205 (2016).

    Article  PubMed  CAS  Google Scholar 

  112. Jones, R. M. et al. Symbiotic lactobacilli stimulate gut epithelial proliferation via Nox-mediated generation of reactive oxygen species. EMBO J. 32, 3017–3028 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  113. Buchon, N. et al. Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep. 3, 1725–1738 (2013).

    Article  PubMed  CAS  Google Scholar 

  114. Marianes, A. & Spalding, A. C. Physiological and stem cell compartmentalization within the Drosophila midgut. Elife 2, e00886 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. Stoffolano, J. G. Jr. & Haselton, A. T. The adult Dipteran crop: a unique and overlooked organ. Annu. Rev. Entomol. 58, 205–225 (2013).

    Article  PubMed  CAS  Google Scholar 

  116. Dow, J. A. Insights into the Malpighian tubule from functional genomics. J. Exp. Biol. 212, 435–445 (2009).

    Article  PubMed  CAS  Google Scholar 

  117. Chintapalli, V. R. et al. Functional correlates of positional and gender–specific renal asymmetry in Drosophila. PLoS One 7, e32577 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

This review was written with the financial support from NIH grant R01GM095372.

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  1. Department of Entomology and Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY, USA

    Angela E. Douglas

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Douglas, A.E. The Drosophila model for microbiome research. Lab Anim 47, 157–164 (2018). https://doi.org/10.1038/s41684-018-0065-0

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