Drosophila Perpetuates Nutritional Mutualism by Promoting the Fitness of Its Intestinal Symbiont Lactobacillus plantarum

Cell Metabolism

Volumn 27, Issue 2, 2018, Pages 362-377.e8

  Storelli, Gilles ^a,c   Strigini, Maura ^a,d   Grenier, Théodore ^a   Bozonnet, Loan ^a   Schwarzer, Martin ^a   Daniel, Catherine ^b   Matos, Renata ^a   Leulier, François ^a  

^a UNIVERSITÉ DE LYON   (France)

^b UNIV LILLE   (France)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITÉ JEAN MONNET   (France)

Author keywords

animal physiology; bacteria; commensalism; Drosophila; growth; Lactobacillus; microbiota; mutualism; nutrition; symbiosis

Indexed keywords

N ACETYLGLUCOSAMINE;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL CELL; BACTERIAL LOAD; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM CULTURE; COLONY FORMING UNIT; COMMENSAL; CONTROLLED STUDY; FRUIT FLY MODEL; GNOTOBIOTICS; INSECT DEVELOPMENT; INSECT LARVA; INTESTINE BRUSH BORDER; INTESTINE CELL; INTESTINE FLORA; LACTOBACILLUS PLANTARUM; LARVAL DEVELOPMENT; LARVAL STAGE; MACRONUTRIENT; METABOLOMICS; NONHUMAN; PRIORITY JOURNAL; PROVENTRICULUS; REARING; SYMBIONT; SYMBIOSIS; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; ANIMAL FOOD; CYTOLOGY; DIET; DROSOPHILA MELANOGASTER; FEEDING BEHAVIOR; GROWTH, DEVELOPMENT AND AGING; INTESTINE; LARVA; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PHYSIOLOGY;

ACETYLGLUCOSAMINE; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; DIET; DROSOPHILA MELANOGASTER; FEEDING BEHAVIOR; INTESTINES; LACTOBACILLUS PLANTARUM; LARVA; MICROBIAL VIABILITY; SYMBIOSIS;

EID: 85043440305     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2017.11.011     Document Type: Article

References (43)

1. Baer, R., Bankier, A.T., Biggin, M.D., Deininger, P.L., Farrell, P.J., Gibson, T.J., Hatfull, G., Hudson, G.S., Satchwell, S.C., Seguin, C., et al. DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature 310 (1984), 207–211.
2. Blaser, M.J., Antibiotic use and its consequences for the normal microbiome. Science 352 (2016), 544–545.
3. Blum, J.E., Fischer, C.N., Miles, J., Handelsman, J., Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster. MBio, 4, 2013 e00860–13.
4. Broderick, N.A., Buchon, N., Lemaitre, B., Microbiota-induced changes in Drosophila melanogaster host gene expression and gut morphology. MBio, 5, 2014 e01117–14.
5. Buchon, N., Broderick, N.A., Lemaitre, B., Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat. Rev. Microbiol. 11 (2013), 615–626.
6. Buchon, N., Osman, D., David, F.P., Fang, H.Y., Boquete, J.P., Deplancke, B., Lemaitre, B., Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep. 3 (2013), 1725–1738.
7. Chaston, J.M., Newell, P.D., Douglas, A.E., Metagenome-wide association of microbial determinants of host phenotype in Drosophila melanogaster. MBio, 5, 2014 e01631–14.
8. Chng, W.B., Bou Sleiman, M.S., Schupfer, F., Lemaitre, B., Transforming growth factor beta/activin signaling functions as a sugar-sensing feedback loop to regulate digestive enzyme expression. Cell Rep. 9 (2014), 336–348.
9. Collins, S.M., Surette, M., Bercik, P., The interplay between the intestinal microbiota and the brain. Nat. Rev. Microbiol. 10 (2012), 735–742.
10. Douglas, A.E., The Symbiotic Habit. 2010, Princeton University Press.
11. Dubreuil, R.R., Copper cells and stomach acid secretion in the Drosophila midgut. Int. J. Biochem. Cell Biol. 36 (2004), 745–752.
12. Erkosar, B., Storelli, G., Defaye, A., Leulier, F., Host-intestinal microbiota mutualism: “learning on the fly”. Cell Host Microbe 13 (2013), 8–14.
13. Erkosar, B., Storelli, G., Mitchell, M., Bozonnet, L., Bozonnet, N., Leulier, F., Pathogen virulence impedes mutualist-mediated enhancement of host juvenile growth via inhibition of protein digestion. Cell Host Microbe 18 (2015), 445–455.
14. Flint, H.J., Scott, K.P., Duncan, S.H., Louis, P., Forano, E., Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3 (2012), 289–306.
15. Gilbert, J.A., Neufeld, J.D., Life in a world without microbes. PLoS Biol., 12, 2014, e1002020.
16. Hickey, D.A., Benkel, B.F., Abukashawa, S., Haus, S., DNA rearrangement causes multiple changes in gene expression at the amylase locus in Drosophila melanogaster. Biochem. Genet. 26 (1988), 757–768.
17. Hooper, L.V., Midtvedt, T., Gordon, J.I., How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu. Rev. Nutr. 22 (2002), 283–307.
18. Hoppler, S., Bienz, M., Specification of a single cell type by a Drosophila homeotic gene. Cell 76 (1994), 689–702.
19. Huang, J.H., Douglas, A.E., Consumption of dietary sugar by gut bacteria determines Drosophila lipid content. Biol. Lett., 11, 2015, 20150469.
20. Lee, W.J., Brey, P.T., How microbiomes influence metazoan development: insights from history and Drosophila modeling of gut-microbe interactions. Annu. Rev. Cell Dev. Biol. 29 (2013), 571–592.
21. Lemaitre, B., Miguel-Aliaga, I., The digestive tract of Drosophila melanogaster. Annu. Rev. Genet. 47 (2013), 377–404.
22. Leulier, F., MacNeil, L.T., Lee, W.J., Rawls, J.F., Cani, P.D., Schwarzer, M., Zhao, L., Simpson, S.J., Integrative physiology: at the crossroads of nutrition, microbiota, animal physiology and human health. Cell Metab. 25 (2017), 522–534.
23. Li, H., Qi, Y., Jasper, H., Preventing age-related decline of gut compartmentalization limits microbiota dysbiosis and extends lifespan. Cell Host Microbe 19 (2016), 240–253.
24. Ma, D., Storelli, G., Mitchell, M., Leulier, F., Studying host-microbiota mutualism in Drosophila: harnessing the power of gnotobiotic flies. Biomed. J. 38 (2015), 285–293.
25. Martino, M.E., Bayjanov, J.R., Caffrey, B.E., Wels, M., Joncour, P., Hughes, S., Gillet, B., Kleerebezem, M., van Hijum, S.A., Leulier, F., Nomadic lifestyle of Lactobacillus plantarum revealed by comparative genomics of 54 strains isolated from different habitats. Environ. Microbiol. 18 (2016), 4974–4989.
26. Matos, R.C., Gervais, H., Joncour, P., Schwarzer, M., Gillet, B., Martino, M.E., Courtin, P., Hughes, S., Chapot-Chartier, M.-P., Leulier, F., D-Alanine esterification of teichoic acids contributes to Lactobacillus plantarum mediated intestinal peptidase expression and Drosophila growth promotion upon chronic undernutrition. Nat. Microbiol., 2017, 10.1038/s41564-017-0038-x.
27. McFall-Ngai, M., Hadfield, M.G., Bosch, T.C., Carey, H.V., Domazet-Loso, T., Douglas, A.E., Dubilier, N., Eberl, G., Fukami, T., Gilbert, S.F., et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 110 (2013), 3229–3236.
28. Mondot, S., de Wouters, T., Dore, J., Lepage, P., The human gut microbiome and its dysfunctions. Dig. Dis. 31 (2013), 278–285.
29. Mushegian, A.A., Ebert, D., Rethinking “mutualism” in diverse host-symbiont communities. Bioessays 38 (2016), 100–108.
30. Nicholson, J.K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., Pettersson, S., Host-gut microbiota metabolic interactions. Science 336 (2012), 1262–1267.
31. Overend, G., Luo, Y., Henderson, L., Douglas, A.E., Davies, S.A., Dow, J.A., Molecular mechanism and functional significance of acid generation in the Drosophila midgut. Sci. Rep., 6, 2016, 27242.
32. Phillips, M.D., Thomas, G.H., Brush border spectrin is required for early endosome recycling in Drosophila. J. Cell Sci. 119 (2006), 1361–1370.
33. Ryu, J.H., Kim, S.H., Lee, H.Y., Bai, J.Y., Nam, Y.D., Bae, J.W., Lee, D.G., Shin, S.C., Ha, E.M., Lee, W.J., Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319 (2008), 777–782.
34. Schneider, C.A., Rasband, W.S., Eliceiri, K.W., NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9 (2012), 671–675.
35. Schwarzer, M., Makki, K., Storelli, G., Machuca-Gayet, I., Srutkova, D., Hermanova, P., Martino, M.E., Balmand, S., Hudcovic, T., Heddi, A., et al. Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science 351 (2016), 854–857.
36. Shanbhag, S., Tripathi, S., Epithelial ultrastructure and cellular mechanisms of acid and base transport in the Drosophila midgut. J. Exp. Biol. 212 (2009), 1731–1744.
37. Sommer, F., Backhed, F., The gut microbiota – masters of host development and physiology. Nat. Rev. Microbiol. 11 (2013), 227–238.
38. Sonnenburg, E.D., Smits, S.A., Tikhonov, M., Higginbottom, S.K., Wingreen, N.S., Sonnenburg, J.L., Diet-induced extinctions in the gut microbiota compound over generations. Nature 529 (2016), 212–215.
39. Storelli, G., Defaye, A., Erkosar, B., Hols, P., Royet, J., Leulier, F., Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR dependent nutrient sensing. Cell Metab. 14 (2011), 403–414.
40. Storey, J.D., Tibshirani, R., Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 100 (2003), 9440–9445.
41. Strand, M., Micchelli, C.A., Quiescent gastric stem cells maintain the adult Drosophila stomach. Proc. Natl. Acad. Sci. USA 108 (2011), 17696–17701.
42. Strigini, M., Leulier, F., The role of the microbial environment in Drosophila post-embryonic development. Dev. Comp. Immunol. 64 (2016), 39–52.
43. Wilson, A.C., Ashton, P.D., Calevro, F., Charles, H., Colella, S., Febvay, G., Jander, G., Kushlan, P.F., Macdonald, S.J., Schwartz, J.F., et al. Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol. Biol. 19:Suppl 2 (2010), 249–258.