Microbial Ecology

, Volume 79, Issue 1, pp 241–251 | Cite as

Taxon-Specific Effects of Lactobacillus on Drosophila Host Development

  • Jaegeun Lee
  • Gangsik Han
  • Jae Woon Kim
  • Che Ok JeonEmail author
  • Seogang HyunEmail author
Host Microbe Interactions


Commensal microbiota heavily influence metazoan host physiology. Drosophila melanogaster has been proven a valuable animal model for studying many aspects of host-microbiota interaction. Lactobacillus are the most common human probiotics and are also one of the major symbiotic bacteria in Drosophila. Although the beneficial effects of Lactobacillus on fly development and physiology have been recognized, how broadly these effects are observed across the Lactobacillus taxa remains largely unknown. In this study, four Lactobacillus species including five strains of L. plantarum were examined for their effects on fly larval development. Monoassociation of germ-free flies with L. rhamnosus (GG) most strongly accelerated fly larval development. Monoassociation with L. plantarum moderately accelerated fly development, but monoassociation with L. reuteri or L. sakei had marginal effects, despite similar bacterial loads in the host gut. An L. plantarum strain previously isolated from our lab rarely enhanced larval development, confirming the strain-specific effects of L. plantarum. The correlation between development-promoting effects and protein digestion activity in the host gut was found only among the members of L. plantarum species. Moreover, the cytoprotective response in the host gut known to be induced by L. plantarum was not correlated with development-promoting effects among any of the bacteria tested. Our results suggest that a broad range of Lactobacillus taxa are able to reside in the fly gut, but their ability to enhance host larval development is highly varied. This study may aid our understanding of the basic principles underlying the beneficial effects of probiotic commensal bacteria on metazoan development.


Host-microbe interaction Drosophila melanogaster Lactobacillus Commensal bacteria Larval development Peptidase expression Cytoprotective response 



We thank Dr. Won-Jae Lee for sharing L. plantarum (WJL) strain. We thank the Bloomington Drosophila Stock Center for the fly stocks used in this study.

Funding Information

This research was supported by the Basic Science Research Program of the National Research Foundation of Korea (NRF), funded by the Ministry of Education, Science, and Technology (Grant Number: 2017R1A2A2A05069502). This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. NRF-2018R1A5A1025077). This research was supported by the Chung-Ang University Graduate Research Scholarship in 2018.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interests.

Supplementary material

248_2019_1404_MOESM1_ESM.pdf (29 kb)
ESM 1 (PDF 28 kb)


  1. 1.
    Hooper LV, Midtvedt T, Gordon JI (2002) How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22:283–307CrossRefGoogle Scholar
  2. 2.
    Erkosar B, Leulier F (2014) Transient adult microbiota, gut homeostasis and longevity: novel insights from the Drosophila model. FEBS Lett 588:4250–4257CrossRefGoogle Scholar
  3. 3.
    Erkosar B, Storelli G, Defaye A, Leulier F (2013) Host-intestinal microbiota mutualism: “learning on the fly”. Cell Host Microbe 13:8–14CrossRefGoogle Scholar
  4. 4.
    Wong AC, Vanhove AS, Watnick PI (2016) The interplay between intestinal bacteria and host metabolism in health and disease: lessons from Drosophila melanogaster. Dis Model Mech 9:271–281CrossRefGoogle Scholar
  5. 5.
    Lhocine N, Ribeiro PS, Buchon N, Wepf A, Wilson R, Tenev T, Lemaitre B, Gstaiger M, Meier P, Leulier F (2008) PIMS modulates immune tolerance by negatively regulating Drosophila innate immune signaling. Cell Host Microbe 4:147–158CrossRefGoogle Scholar
  6. 6.
    Bosco-Drayon V, Poidevin M, Boneca IG, Narbonne-Reveau K, Royet J, Charroux B (2012) Peptidoglycan sensing by the receptor PGRP-LE in the Drosophila gut induces immune responses to infectious bacteria and tolerance to microbiota. Cell Host Microbe 12:153–165CrossRefGoogle Scholar
  7. 7.
    Bischoff V, Vignal C, Duvic B, Boneca IG, Hoffmann JA, Royet J (2006) Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. PLoS Pathog 2:e14CrossRefGoogle Scholar
  8. 8.
    Buchon N, Broderick NA, Chakrabarti S, Lemaitre B (2009) Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev 23:2333–2344CrossRefGoogle Scholar
  9. 9.
    Ha EM, Lee KA, Seo YY, Kim SH, Lim JH, Oh BH, Kim J, Lee WJ (2009) Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in drosophila gut. Nat Immunol 10:949–957CrossRefGoogle Scholar
  10. 10.
    Paredes JC, Welchman DP, Poidevin M, Lemaitre B (2011) Negative regulation by amidase PGRPs shapes the Drosophila antibacterial response and protects the fly from innocuous infection. Immunity 35:770–779CrossRefGoogle Scholar
  11. 11.
    Ryu JH, Kim SH, Lee HY, Bai JY, Nam YD, Bae JW, Lee DG, Shin SC, Ha EM, Lee WJ (2008) Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319:777–782CrossRefGoogle Scholar
  12. 12.
    Guo L, Karpac J, Tran SL, Jasper H (2014) PGRP-SC2 promotes gut immune homeostasis to limit commensal dysbiosis and extend lifespan. Cell 156:109–122CrossRefGoogle Scholar
  13. 13.
    Broderick NA, Lemaitre B (2012) Gut-associated microbes of Drosophila melanogaster. Gut Microbes 3:307–321CrossRefGoogle Scholar
  14. 14.
    Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 14:403–414CrossRefGoogle Scholar
  15. 15.
    Cox CR, Gilmore MS (2007) Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infect Immun 75:1565–1576CrossRefGoogle Scholar
  16. 16.
    Ren C, Webster P, Finkel SE, Tower J (2007) Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metab 6:144–152CrossRefGoogle Scholar
  17. 17.
    Wong CN, Ng P, Douglas AE (2011) Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environ Microbiol 13:1889–1900CrossRefGoogle Scholar
  18. 18.
    Erkosar B, Storelli G, Mitchell M, Bozonnet L, Bozonnet N, Leulier F (2015) Pathogen virulence impedes mutualist-mediated enhancement of host juvenile growth via inhibition of protein digestion. Cell Host Microbe 18:445–455CrossRefGoogle Scholar
  19. 19.
    Matos RC, Schwarzer M, Gervais H, Courtin P, Joncour P, Gillet B, Ma D, Bulteau AL, Martino ME, Hughes S, Chapot-Chartier MP, Leulier F (2017) D-Alanylation of teichoic acids contributes to Lactobacillus plantarum-mediated Drosophila growth during chronic undernutrition. Nat Microbiol 2:1635–1647CrossRefGoogle Scholar
  20. 20.
    Jones RM, Luo L, Ardita CS, Richardson AN, Kwon YM, Mercante JW, Alam A, Gates CL, Wu H, Swanson PA, Lambeth JD, Denning PW, Neish AS (2013) Symbiotic lactobacilli stimulate gut epithelial proliferation via Nox-mediated generation of reactive oxygen species. EMBO J 32:3017–3028CrossRefGoogle Scholar
  21. 21.
    Jones RM, Desai C, Darby TM, Luo L, Wolfarth AA, Scharer CD, Ardita CS, Reedy AR, Keebaugh ES, Neish AS (2015) Lactobacilli modulate epithelial cytoprotection through the Nrf2 pathway. Cell Rep 12:1217–1225CrossRefGoogle Scholar
  22. 22.
    Schwarzer M, Makki K, Storelli G, Machuca-Gayet I, Srutkova D, Hermanova P, Martino ME, Balmand S, Hudcovic T, Heddi A, Rieusset J, Kozakova H, Vidal H, Leulier F (2016) Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science 351:854–857CrossRefGoogle Scholar
  23. 23.
    Han G, Lee HJ, Jeong SE, Jeon CO, Hyun S (2017) Comparative analysis of Drosophila melanogaster gut microbiota with respect to host strain, sex, and age. Microb Ecol 74:207–216CrossRefGoogle Scholar
  24. 24.
    Sannino DR, Dobson AJ, Edwards K, Angert ER, Buchon N (2018) The Drosophila melanogaster gut microbiota provisions thiamine to its host. MBio 9:e00155–e00118CrossRefGoogle Scholar
  25. 25.
    Keebaugh ES, Yamada R, Obadia B, Ludington WB, Ja WW (2018) Microbial quantity impacts Drosophila nutrition, development, and lifespan. iScience 4:247–259CrossRefGoogle Scholar
  26. 26.
    Yamada R, Deshpande SA, Bruce KD, Mak EM, Ja WW (2015) Microbes promote amino acid harvest to rescue undernutrition in Drosophila. Cell Rep 10:865–872CrossRefGoogle Scholar
  27. 27.
    Blum JE, Fischer CN, Miles J, Handelsman J (2013) Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster. MBio 4:e00860–e00813CrossRefGoogle Scholar
  28. 28.
    Shin SC, Kim SH, You H, Kim B, Kim AC, Lee KA, Yoon JH, Ryu JH, Lee WJ (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334:670–674CrossRefGoogle Scholar
  29. 29.
    Kechagia M, Basoulis D, Konstantopoulou S, Dimitriadi D, Gyftopoulou K, Skarmoutsou N, Fakiri EM (2013) Health benefits of probiotics: a review. ISRN nutrition 2013:481651CrossRefGoogle Scholar
  30. 30.
    George Kerry R, Patra JK, Gouda S, Park Y, Shin HS, Das G (2018) Benefaction of probiotics for human health: a review. J Food Drug Anal 26:927–939CrossRefGoogle Scholar
  31. 31.
    Lee ES, Song EJ, Nam YD, Lee SY (2018) Probiotics in human health and disease: from nutribiotics to pharmabiotics. J Microbiol 56:773–782CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Life ScienceChung-Ang UniversitySeoulRepublic of Korea

Personalised recommendations