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Microbiome in the Drosophila gut

May 15, 2024

The microbiota are the sum of all symbiotic microorganisms (mutualistic, commensal or pathogenic) living on or in an organism. The fruit fly Drosophila melanogaster is a model organism and known as one of the most investigated organisms worldwide. The microbiota in flies is less complex than that found in humans. It still has an influence on the fitness of the fly,[1] and it affects different life-history characteristics such as lifespan (life expectancy), resistance against pathogens (immunity) and metabolic processes (digestion). Considering the comprehensive toolkit available for research in Drosophila, analysis of its microbiome could enhance our understanding of similar processes in other types of host-microbiota interactions, including those involving humans. Microbiota plays key roles in the intestinal immune and metabolic responses via their fermentation product (short chain fatty acid), acetate.[2]

Microbial composition edit

Drosophila melanogaster possesses a comparatively simple gut microbiota, consisting of only few bacterial species, mainly from two bacterial taxonomic groups: Bacillota and Pseudomonadota.[3][4] The most common species belong to the families Lactobacillaceae (abundance of approx. 30%, members of the Bacillota) and Acetobacteraceae (approx. 55%, members of the Proteobacteria). Other less common bacterial species are from the families Leuconostocaceae, Enterococceae, and Enterobacteriaceae (all with an abundance in between 2–4%).[4] The most common species include Lactobacillus plantarum, Lactobacillus brevis, Acetobacter pomorum and Enterococcus faecalis, while other species such as Acetobacter aceti, Acetobacter tropicalis and Acetobacter pasteurianus are also often found.[3]

The particular species of the host fly has a central influence on the composition and quality of the gut microbiota, even if flies are raised under similar conditions.[5] Nevertheless, the host's diet and nutritional environment also shape the exact composition of the microbiota. For instance the exact pH of the food can kill certain bacterial species.[3] In general, the type of food used by the fly affects the microbiota composition.[6] Mushroom feeder species like Drosophila falleni and Microdrosophila harbour many Lactobacillales and generally maintain high bacterial diversity in their guts. The microbiota of flower feeders such as Drosophila elegans and Drosophila flavohirta shows higher abundance of Enterobacteriaceae and to a lesser extent of acido-philic bacteria (such as Acetobacteraceae and Lactobacillaceae) if compared to fruit-eating species such as Drosophila hydei, Drosophila immigrans, Drosophila sulfurigaster, Drosophila melanogaster, Drosophila sechellia or Drosophila takahashii.[3] The microbial load and bacterial composition also vary with the age of the host fly.[3]

Microbiota transmission and establishment edit

Feeding is a key determinant of the microbiota composition. Not only the diet influences presence and abundance of the bacteria inside the gut, but the bacteria also need to be taken up continuously from the environment to prevail as members of the intestinal flora.[7] Feeding on feces seems to play a central role for establishment of the Drosophila microbiota, as it allows the flies to recycle the bacteria within a fly population at a particular time point and also across generations. Flies seed the embryonic eggshell with feces. Upon hatching, young larvae eat their eggshells and thereby pick up the bacteria. The microbiota, which subsequently establishes itself inside the gut of the developing larvae, is similar to that of the larvae's mothers.[8] This may further be promoted by the particular life history of the flies. Young adult flies, which harbor fewer bacteria than old flies, proliferate in an environment shaped by the feces of the preceding fly generation, thus allowing them to take up additional bacteria.[8]

Gut compartmentalization edit

In the gut of Drosophila melanogaster the composition and action of the microbiome appears to be tightly regulated within compartments, that is different sections of the intestines. This is indicated by the differential expression of genes, especially with a regulatory function, in the epithelium of different parts of the gut. In detail, the gut is compartmentalized into three parts, the foregut, the midgut, and the hindgut. While foregut and hindgut are lined with a cuticle formed by the ectodermal epithelium, the midgut is of endodermal origin.[9] In adult flies the midgut is further divided into five smaller regions.[10] The immune response varies among the gut regions. The immune deficiency (IMD) pathway responds to bacterial infections and is activated by certain receptors (e.g., the peptidoglycan receptor protein PGRP-LC). These receptors and also other components of the Drosophila immune system such as Toll receptor and dDUOX pathway molecules control immune responses in ectodermal tissue of the anterior gut. Moreover, the anterior midgut is enriched in certain antimicrobial peptides (AMPs). This suggests that the immune defence in this area is particularly responsive, possibly because this regions represents the first contact region for newly taken up food, microbiota, and/or intestinal pathogens. In the middle and posterior midgut, other genes such as the receptor PGRP-LB, which down-regulates the IMD immune response, are expressed, possibly in order to minimize expression of immune defence against the microbiota. In addition, the microbiota itself seems to control the expression of several Drosophila metabolic genes within the midgut, possibly to facilitate digestion of food.[11] Recently, IMD pathway in the anterior midgut region has been proposed to play multi-pronged roles to modulate key metabolic and mechanic functions in the gut.[12] Taken together, it appears that the interaction between host and microbiota is precisely regulated across different regions within the gut.[13]

Effects on behaviour edit

Drosophila microbiota have been implicated in mating success by influencing assortative mating; a phenomenon detected in some studies of Drosophila,[14] but not others.[15]

Effects on longevity edit

The microbiota seem to affect the lifespan of Drosophila melanogaster. To date, the mechanisms of this effect remain elusive.
Fruit flies raised under axenic conditions (i.e., without any bacteria in the environment) or cured of their microbiota with antibiotics had a shorter lifespan than flies raised under normal conditions. The microbiota influence on longevity seems to be particularly strong early in development.[16] To date, however, the exact mechanisms underlying these effects remain elusive. It is possible that the microbiota-induced proliferation of intestinal stem cells and associated metabolic homeostasis is important in this context.[17] In contrast, the microbiota seems to have a negative effect on lifespan in older Drosophila melanogaster, because their removal in ageing flies increases longevity. Old flies have a reduced ability to fight infections and this may also relate to the bacterial members of the microbiota.[18] In aged animals, immune responses may over-shoot, possibly harming the host and favoring colonization with pathogens (e.g. Gluconobacter morbifer).[19]

New methods of microbiome analysis edit

Almost all current approaches for the characterization of Drosophila microbiota rely on destructive approaches, that is flies are killed, their gut is extracted and from these the bacteria are isolated and/or analyzed. For an assessment of microbiota dynamics across the lifespan of an individual fly or across development of a fly population, a non-destructive approach would be favorable. Such an approach was recently developed, focusing on the microbial characterization of fly feces. Fly feces are indeed informative on composition of the gut microbiota, since the diversity of gut bacteria, feces bacteria and bacteria of whole fly of Drosophila melanogaster are all strongly correlated. This new approach could be used to demonstrate the known influence of diets.[20]

References edit

  1. ^ Gould AL, Zhang V, Lamberti L, Jones EW, Obadia B, Korasidis N, et al. (December 2018). "Microbiome interactions shape host fitness". Proceedings of the National Academy of Sciences of the United States of America. 115 (51): E11951–E11960. Bibcode:2018PNAS..11511951G. doi:10.1073/pnas.1809349115. PMC 6304949. PMID 30510004.
  2. ^ Jugder, Bat-Erdene; Kamareddine, Layla; Watnick, Paula I. (2021). "Microbiota-derived acetate activates intestinal innate immunity via the Tip60 histone acetyltransferase complex". Immunity. 54 (8): 1683–1697.e3. doi:10.1016/j.immuni.2021.05.017. ISSN 1074-7613. PMC 8363570. PMID 34107298.
  3. ^ a b c d e Erkosar B, Storelli G, Defaye A, Leulier F (January 2013). "Host-intestinal microbiota mutualism: "learning on the fly"". Cell Host & Microbe. 13 (1): 8–14. doi:10.1016/j.chom.2012.12.004. PMID 23332152.
  4. ^ a b Staubach F, Baines JF, Künzel S, Bik EM, Petrov DA (2013). "Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment". PLOS ONE. 8 (8): e70749. arXiv:1211.3367. Bibcode:2013PLoSO...870749S. doi:10.1371/journal.pone.0070749. PMC 3742674. PMID 23967097.
  5. ^ Broderick NA, Lemaitre B (2012). "Gut-associated microbes of Drosophila melanogaster". Gut Microbes. 3 (4): 307–21. doi:10.4161/gmic.19896. PMC 3463489. PMID 22572876.
  6. ^ Chandler JA, Lang JM, Bhatnagar S, Eisen JA, Kopp A (September 2011). "Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system". PLOS Genetics. 7 (9): e1002272. doi:10.1371/journal.pgen.1002272. PMC 3178584. PMID 21966276.
  7. ^ Storelli G, Strigini M, Grenier T, Bozonnet L, Schwarzer M, Daniel C, Matos R, Leulier F (February 2018). "Drosophila Perpetuates Nutritional Mutualism by Promoting the Fitness of Its Intestinal Symbiont Lactobacillus plantarum". Cell Metab. 27 (2): 362–377. doi:10.1016/j.cmet.2017.11.011. PMC 5807057. PMID 29290388.
  8. ^ a b Blum JE, Fischer CN, Miles J, Handelsman J (November 2013). "Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster". mBio. 4 (6): e00860-13. doi:10.1128/mbio.00860-13. PMC 3892787. PMID 24194543.
  9. ^ Lemaitre B, Miguel-Aliaga I (2013). "The digestive tract of Drosophila melanogaster". Annual Review of Genetics. 47: 377–404. doi:10.1146/annurev-genet-111212-133343. PMID 24016187.
  10. ^ Buchon N, Osman D, David FP, Fang HY, Boquete JP, Deplancke B, Lemaitre B (May 2013). "Morphological and molecular characterization of adult midgut compartmentalization in Drosophila". Cell Reports. 3 (5): 1725–38. doi:10.1016/j.celrep.2013.04.001. PMID 23643535.
  11. ^ Broderick NA, Buchon N, Lemaitre B (May 2014). "Microbiota-induced changes in Drosophila melanogaster host gene expression and gut morphology". mBio. 5 (3): e01117-14. doi:10.1128/mbio.01117-14. PMC 4045073. PMID 24865556.
  12. ^ Watnick PI, Jugder BE (February 2020). "Microbial Control of Intestinal Homeostasis via Enteroendocrine Cell Innate Immune Signaling". Trends in Microbiology. 28 (2): 141–149. doi:10.1016/j.tim.2019.09.005. PMC 6980660. PMID 31699645.
  13. ^ Bosco-Drayon V, Poidevin M, Boneca IG, Narbonne-Reveau K, Royet J, Charroux B (August 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 (2): 153–65. doi:10.1016/j.chom.2012.06.002. PMID 22901536.
  14. ^ Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E (November 2010). "Commensal bacteria play a role in mating preference of Drosophila melanogaster". Proceedings of the National Academy of Sciences of the United States of America. 107 (46): 20051–6. doi:10.1073/pnas.1009906107. PMC 2993361. PMID 21041648.
  15. ^
    • Leftwich PT, Clarke NV, Hutchings MI, Chapman T (November 2017). "Drosophila". Proceedings of the National Academy of Sciences of the United States of America. 114 (48): 12767–12772. doi:10.1073/pnas.1708345114. PMC 5715749. PMID 29109277.
    • Miguel-Aliaga, Irene; Jasper, Heinrich; Lemaitre, Bruno (2018-10-01). "Anatomy and Physiology of the Digestive Tract of Drosophila melanogaster". Genetics. 210 (2). Genetics Society of America (OUP): 357–396. doi:10.1534/genetics.118.300224. ISSN 1943-2631. PMC 6216580. PMID 30287514. S2CID 52922044.
    • Douglas, Angela E. (2019-08-15). "Simple animal models for microbiome research". Nature Reviews Microbiology. 17 (12): 764–775. doi:10.1038/s41579-019-0242-1. ISSN 1740-1534. PMID 31417197. S2CID 199661914. (AED ORCID: 0000-0001-5212-6826).
    • Leftwich PT, Hutchings MI, Chapman T (December 2018). "Diet, Gut Microbes and Host Mate Choice: Understanding the significance of microbiome effects on host mate choice requires a case by case evaluation". BioEssays. 40 (12): e1800053. doi:10.1002/bies.201800053. PMID 30311675.
    • Cusick, Jessica A.; Wellman, Cara L.; Demas, Gregory E. (2021-05-14). "The call of the wild: using non-model systems to investigate microbiome–behaviour relationships". Journal of Experimental Biology. 224 (10). The Company of Biologists. doi:10.1242/jeb.224485. ISSN 0022-0949. PMC 8180253. PMID 33988717. S2CID 234497490.
  16. ^ Brummel T, Ching A, Seroude L, Simon AF, Benzer S (August 2004). "Drosophila lifespan enhancement by exogenous bacteria". Proceedings of the National Academy of Sciences of the United States of America. 101 (35): 12974–9. Bibcode:2004PNAS..10112974B. doi:10.1073/pnas.0405207101. PMC 516503. PMID 15322271.
  17. ^ Shin SC, Kim SH, You H, Kim B, Kim AC, Lee KA, et al. (November 2011). "Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling". Science. 334 (6056): 670–4. Bibcode:2011Sci...334..670S. doi:10.1126/science.1212782. PMID 22053049. S2CID 206536986.
  18. ^ Ramsden S, Cheung YY, Seroude L (March 2008). "Functional analysis of the Drosophila immune response during aging". Aging Cell. 7 (2): 225–36. doi:10.1111/j.1474-9726.2008.00370.x. PMID 18221416. S2CID 8510421.
  19. ^ Ryu JH, Kim SH, Lee HY, Bai JY, Nam YD, Bae JW, et al. (February 2008). "Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila". Science. 319 (5864): 777–82. Bibcode:2008Sci...319..777R. doi:10.1126/science.1149357. PMID 18218863. S2CID 23798836.
  20. ^ Fink C, Staubach F, Kuenzel S, Baines JF, Roeder T (November 2013). "Noninvasive analysis of microbiome dynamics in the fruit fly Drosophila melanogaster". Applied and Environmental Microbiology. 79 (22): 6984–8. Bibcode:2013ApEnM..79.6984F. doi:10.1128/AEM.01903-13. PMC 3811555. PMID 24014528.

External links edit

  • Erkosar B, Storelli G, Defaye A, Leulier F (January 2013). "Host-intestinal microbiota mutualism: "learning on the fly"". Cell Host & Microbe. 13 (1): 8–14. doi:10.1016/j.chom.2012.12.004. PMID 23332152.
  • Erkosar B, Leulier F (November 2014). "Transient adult microbiota, gut homeostasis and longevity: novel insights from the Drosophila model". FEBS Letters. 588 (22): 4250–7. doi:10.1016/j.febslet.2014.06.041. PMID 24983497. S2CID 5423153.
  • Fink C, Staubach F, Kuenzel S, Baines JF, Roeder T (November 2013). "Noninvasive analysis of microbiome dynamics in the fruit fly Drosophila melanogaster". Applied and Environmental Microbiology. 79 (22): 6984–8. Bibcode:2013ApEnM..79.6984F. doi:10.1128/AEM.01903-13. PMC 3811555. PMID 24014528.

May 15, 2024
microbiome, drosophila, microbiota, symbiotic, microorganisms, mutualistic, commensal, pathogenic, living, organism, fruit, drosophila, melanogaster, model, organism, known, most, investigated, organisms, worldwide, microbiota, flies, less, complex, than, that. The microbiota are the sum of all symbiotic microorganisms mutualistic commensal or pathogenic living on or in an organism The fruit fly Drosophila melanogaster is a model organism and known as one of the most investigated organisms worldwide The microbiota in flies is less complex than that found in humans It still has an influence on the fitness of the fly 1 and it affects different life history characteristics such as lifespan life expectancy resistance against pathogens immunity and metabolic processes digestion Considering the comprehensive toolkit available for research in Drosophila analysis of its microbiome could enhance our understanding of similar processes in other types of host microbiota interactions including those involving humans Microbiota plays key roles in the intestinal immune and metabolic responses via their fermentation product short chain fatty acid acetate 2 Contents 1 Microbial composition 2 Microbiota transmission and establishment 3 Gut compartmentalization 4 Effects on behaviour 5 Effects on longevity 6 New methods of microbiome analysis 7 References 8 External linksMicrobial composition editDrosophila melanogaster possesses a comparatively simple gut microbiota consisting of only few bacterial species mainly from two bacterial taxonomic groups Bacillota and Pseudomonadota 3 4 The most common species belong to the families Lactobacillaceae abundance of approx 30 members of the Bacillota and Acetobacteraceae approx 55 members of the Proteobacteria Other less common bacterial species are from the families Leuconostocaceae Enterococceae and Enterobacteriaceae all with an abundance in between 2 4 4 The most common species include Lactobacillus plantarum Lactobacillus brevis Acetobacter pomorum and Enterococcus faecalis while other species such as Acetobacter aceti Acetobacter tropicalis and Acetobacter pasteurianus are also often found 3 The particular species of the host fly has a central influence on the composition and quality of the gut microbiota even if flies are raised under similar conditions 5 Nevertheless the host s diet and nutritional environment also shape the exact composition of the microbiota For instance the exact pH of the food can kill certain bacterial species 3 In general the type of food used by the fly affects the microbiota composition 6 Mushroom feeder species like Drosophila falleni and Microdrosophila harbour many Lactobacillales and generally maintain high bacterial diversity in their guts The microbiota of flower feeders such as Drosophila elegans and Drosophila flavohirta shows higher abundance of Enterobacteriaceae and to a lesser extent of acido philic bacteria such as Acetobacteraceae and Lactobacillaceae if compared to fruit eating species such as Drosophila hydei Drosophila immigrans Drosophila sulfurigaster Drosophila melanogaster Drosophila sechellia or Drosophila takahashii 3 The microbial load and bacterial composition also vary with the age of the host fly 3 Microbiota transmission and establishment editFeeding is a key determinant of the microbiota composition Not only the diet influences presence and abundance of the bacteria inside the gut but the bacteria also need to be taken up continuously from the environment to prevail as members of the intestinal flora 7 Feeding on feces seems to play a central role for establishment of the Drosophila microbiota as it allows the flies to recycle the bacteria within a fly population at a particular time point and also across generations Flies seed the embryonic eggshell with feces Upon hatching young larvae eat their eggshells and thereby pick up the bacteria The microbiota which subsequently establishes itself inside the gut of the developing larvae is similar to that of the larvae s mothers 8 This may further be promoted by the particular life history of the flies Young adult flies which harbor fewer bacteria than old flies proliferate in an environment shaped by the feces of the preceding fly generation thus allowing them to take up additional bacteria 8 Gut compartmentalization editIn the gut of Drosophila melanogaster the composition and action of the microbiome appears to be tightly regulated within compartments that is different sections of the intestines This is indicated by the differential expression of genes especially with a regulatory function in the epithelium of different parts of the gut In detail the gut is compartmentalized into three parts the foregut the midgut and the hindgut While foregut and hindgut are lined with a cuticle formed by the ectodermal epithelium the midgut is of endodermal origin 9 In adult flies the midgut is further divided into five smaller regions 10 The immune response varies among the gut regions The immune deficiency IMD pathway responds to bacterial infections and is activated by certain receptors e g the peptidoglycan receptor protein PGRP LC These receptors and also other components of the Drosophila immune system such as Toll receptor and dDUOX pathway molecules control immune responses in ectodermal tissue of the anterior gut Moreover the anterior midgut is enriched in certain antimicrobial peptides AMPs This suggests that the immune defence in this area is particularly responsive possibly because this regions represents the first contact region for newly taken up food microbiota and or intestinal pathogens In the middle and posterior midgut other genes such as the receptor PGRP LB which down regulates the IMD immune response are expressed possibly in order to minimize expression of immune defence against the microbiota In addition the microbiota itself seems to control the expression of several Drosophila metabolic genes within the midgut possibly to facilitate digestion of food 11 Recently IMD pathway in the anterior midgut region has been proposed to play multi pronged roles to modulate key metabolic and mechanic functions in the gut 12 Taken together it appears that the interaction between host and microbiota is precisely regulated across different regions within the gut 13 Effects on behaviour editDrosophila microbiota have been implicated in mating success by influencing assortative mating a phenomenon detected in some studies of Drosophila 14 but not others 15 Effects on longevity editThe microbiota seem to affect the lifespan of Drosophila melanogaster To date the mechanisms of this effect remain elusive Fruit flies raised under axenic conditions i e without any bacteria in the environment or cured of their microbiota with antibiotics had a shorter lifespan than flies raised under normal conditions The microbiota influence on longevity seems to be particularly strong early in development 16 To date however the exact mechanisms underlying these effects remain elusive It is possible that the microbiota induced proliferation of intestinal stem cells and associated metabolic homeostasis is important in this context 17 In contrast the microbiota seems to have a negative effect on lifespan in older Drosophila melanogaster because their removal in ageing flies increases longevity Old flies have a reduced ability to fight infections and this may also relate to the bacterial members of the microbiota 18 In aged animals immune responses may over shoot possibly harming the host and favoring colonization with pathogens e g Gluconobacter morbifer 19 New methods of microbiome analysis editAlmost all current approaches for the characterization of Drosophila microbiota rely on destructive approaches that is flies are killed their gut is extracted and from these the bacteria are isolated and or analyzed For an assessment of microbiota dynamics across the lifespan of an individual fly or across development of a fly population a non destructive approach would be favorable Such an approach was recently developed focusing on the microbial characterization of fly feces Fly feces are indeed informative on composition of the gut microbiota since the diversity of gut bacteria feces bacteria and bacteria of whole fly of Drosophila melanogaster are all strongly correlated This new approach could be used to demonstrate the known influence of diets 20 References edit Gould AL Zhang V Lamberti L Jones EW Obadia B Korasidis N et al December 2018 Microbiome interactions shape host fitness Proceedings of the National Academy of Sciences of the United States of America 115 51 E11951 E11960 Bibcode 2018PNAS 11511951G doi 10 1073 pnas 1809349115 PMC 6304949 PMID 30510004 Jugder Bat Erdene Kamareddine Layla Watnick Paula I 2021 Microbiota derived acetate activates intestinal innate immunity via the Tip60 histone acetyltransferase complex Immunity 54 8 1683 1697 e3 doi 10 1016 j immuni 2021 05 017 ISSN 1074 7613 PMC 8363570 PMID 34107298 a b c d e Erkosar B Storelli G Defaye A Leulier F January 2013 Host intestinal microbiota mutualism learning on the fly Cell Host amp Microbe 13 1 8 14 doi 10 1016 j chom 2012 12 004 PMID 23332152 a b Staubach F Baines JF Kunzel S Bik EM Petrov DA 2013 Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment PLOS ONE 8 8 e70749 arXiv 1211 3367 Bibcode 2013PLoSO 870749S doi 10 1371 journal pone 0070749 PMC 3742674 PMID 23967097 Broderick NA Lemaitre B 2012 Gut associated microbes of Drosophila melanogaster Gut Microbes 3 4 307 21 doi 10 4161 gmic 19896 PMC 3463489 PMID 22572876 Chandler JA Lang JM Bhatnagar S Eisen JA Kopp A September 2011 Bacterial communities of diverse Drosophila species ecological context of a host microbe model system PLOS Genetics 7 9 e1002272 doi 10 1371 journal pgen 1002272 PMC 3178584 PMID 21966276 Storelli G Strigini M Grenier T Bozonnet L Schwarzer M Daniel C Matos R Leulier F February 2018 Drosophila Perpetuates Nutritional Mutualism by Promoting the Fitness of Its Intestinal Symbiont Lactobacillus plantarum Cell Metab 27 2 362 377 doi 10 1016 j cmet 2017 11 011 PMC 5807057 PMID 29290388 a b Blum JE Fischer CN Miles J Handelsman J November 2013 Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster mBio 4 6 e00860 13 doi 10 1128 mbio 00860 13 PMC 3892787 PMID 24194543 Lemaitre B Miguel Aliaga I 2013 The digestive tract of Drosophila melanogaster Annual Review of Genetics 47 377 404 doi 10 1146 annurev genet 111212 133343 PMID 24016187 Buchon N Osman D David FP Fang HY Boquete JP Deplancke B Lemaitre B May 2013 Morphological and molecular characterization of adult midgut compartmentalization in Drosophila Cell Reports 3 5 1725 38 doi 10 1016 j celrep 2013 04 001 PMID 23643535 Broderick NA Buchon N Lemaitre B May 2014 Microbiota induced changes in Drosophila melanogaster host gene expression and gut morphology mBio 5 3 e01117 14 doi 10 1128 mbio 01117 14 PMC 4045073 PMID 24865556 Watnick PI Jugder BE February 2020 Microbial Control of Intestinal Homeostasis via Enteroendocrine Cell Innate Immune Signaling Trends in Microbiology 28 2 141 149 doi 10 1016 j tim 2019 09 005 PMC 6980660 PMID 31699645 Bosco Drayon V Poidevin M Boneca IG Narbonne Reveau K Royet J Charroux B August 2012 Peptidoglycan sensing by the receptor PGRP LE in the Drosophila gut induces immune responses to infectious bacteria and tolerance to microbiota Cell Host amp Microbe 12 2 153 65 doi 10 1016 j chom 2012 06 002 PMID 22901536 Sharon G Segal D Ringo JM Hefetz A Zilber Rosenberg I Rosenberg E November 2010 Commensal bacteria play a role in mating preference of Drosophila melanogaster Proceedings of the National Academy of Sciences of the United States of America 107 46 20051 6 doi 10 1073 pnas 1009906107 PMC 2993361 PMID 21041648 Leftwich PT Clarke NV Hutchings MI Chapman T November 2017 Drosophila Proceedings of the National Academy of Sciences of the United States of America 114 48 12767 12772 doi 10 1073 pnas 1708345114 PMC 5715749 PMID 29109277 Miguel Aliaga Irene Jasper Heinrich Lemaitre Bruno 2018 10 01 Anatomy and Physiology of the Digestive Tract of Drosophila melanogaster Genetics 210 2 Genetics Society of America OUP 357 396 doi 10 1534 genetics 118 300224 ISSN 1943 2631 PMC 6216580 PMID 30287514 S2CID 52922044 Douglas Angela E 2019 08 15 Simple animal models for microbiome research Nature Reviews Microbiology 17 12 764 775 doi 10 1038 s41579 019 0242 1 ISSN 1740 1534 PMID 31417197 S2CID 199661914 AED ORCID 0000 0001 5212 6826 Leftwich PT Hutchings MI Chapman T December 2018 Diet Gut Microbes and Host Mate Choice Understanding the significance of microbiome effects on host mate choice requires a case by case evaluation BioEssays 40 12 e1800053 doi 10 1002 bies 201800053 PMID 30311675 Cusick Jessica A Wellman Cara L Demas Gregory E 2021 05 14 The call of the wild using non model systems to investigate microbiome behaviour relationships Journal of Experimental Biology 224 10 The Company of Biologists doi 10 1242 jeb 224485 ISSN 0022 0949 PMC 8180253 PMID 33988717 S2CID 234497490 Brummel T Ching A Seroude L Simon AF Benzer S August 2004 Drosophila lifespan enhancement by exogenous bacteria Proceedings of the National Academy of Sciences of the United States of America 101 35 12974 9 Bibcode 2004PNAS 10112974B doi 10 1073 pnas 0405207101 PMC 516503 PMID 15322271 Shin SC Kim SH You H Kim B Kim AC Lee KA et al November 2011 Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling Science 334 6056 670 4 Bibcode 2011Sci 334 670S doi 10 1126 science 1212782 PMID 22053049 S2CID 206536986 Ramsden S Cheung YY Seroude L March 2008 Functional analysis of the Drosophila immune response during aging Aging Cell 7 2 225 36 doi 10 1111 j 1474 9726 2008 00370 x PMID 18221416 S2CID 8510421 Ryu JH Kim SH Lee HY Bai JY Nam YD Bae JW et al February 2008 Innate immune homeostasis by the homeobox gene caudal and commensal gut mutualism in Drosophila Science 319 5864 777 82 Bibcode 2008Sci 319 777R doi 10 1126 science 1149357 PMID 18218863 S2CID 23798836 Fink C Staubach F Kuenzel S Baines JF Roeder T November 2013 Noninvasive analysis of microbiome dynamics in the fruit fly Drosophila melanogaster Applied and Environmental Microbiology 79 22 6984 8 Bibcode 2013ApEnM 79 6984F doi 10 1128 AEM 01903 13 PMC 3811555 PMID 24014528 External links editErkosar B Storelli G Defaye A Leulier F January 2013 Host intestinal microbiota mutualism learning on the fly Cell Host amp Microbe 13 1 8 14 doi 10 1016 j chom 2012 12 004 PMID 23332152 Erkosar B Leulier F November 2014 Transient adult microbiota gut homeostasis and longevity novel insights from the Drosophila model FEBS Letters 588 22 4250 7 doi 10 1016 j febslet 2014 06 041 PMID 24983497 S2CID 5423153 Fink C Staubach F Kuenzel S Baines JF Roeder T November 2013 Noninvasive analysis of microbiome dynamics in the fruit fly Drosophila melanogaster Applied and Environmental Microbiology 79 22 6984 8 Bibcode 2013ApEnM 79 6984F doi 10 1128 AEM 01903 13 PMC 3811555 PMID 24014528 Retrieved from https en wikipedia org w index php title Microbiome in the 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