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Microbiome in the Drosophila gut

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The microbiota describes the sum of all symbiotic microorganisms (mutualism, commensalism 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.

Microbial composition

Drosophila melanogaster possesses a comparatively simple gut microbiota, consisting of only few bacterial species, mainly from two bacterial taxonomic groups: Firmicutes and Proteobacteria.[2][3] The most common species belong to the families Lactobacillaceae (abundance of approx. 30%, members of the Firmicutes) 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%).[3] 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.[2]

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.[4] 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.[2] In general, the type of food used by the fly affects the microbiota composition.[5] Mushroom feeder species like Drosophila fallen and MicroDrosophila sp. 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.[2] The microbial load and bacterial composition also vary with the age of the host fly.[2]

Microbiota transmission and establishment

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. 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.[6] 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.[6]

Gut compartmentalization

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 entodermal origin.[7] In adult flies the midgut is further divided into five smaller regions.[8] 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.[9] 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.[10] Taken together, it appears that the interaction between host and microbiota is precisely regulated across different regions within the gut.[11]

Effects on behaviour

Drosophila microbiota have been implicated in mating success by influencing assortative mating; a phenomenon detected in some studies of Drosophila,[12] but not others[13][14]

Effects on longevity

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.[15] 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.[16] In contrast, the microbiota seems to have a negative effect on lifespan in old 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.[17] In aged animals, immune responses may over-shoot, possibly harming the host and favoruing colonization with pathogens (e.g. Gluconobacter morbifer).[18]

New method of microbiome analysis

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.[19]

References

  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. doi:10.1073/pnas.1809349115. PMC 6304949. PMID 30510004.
  2. ^ 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.
  3. ^ 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.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  4. ^ 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.
  5. ^ 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.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  6. ^ 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.
  7. ^ 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.
  8. ^ 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.
  9. ^ 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.
  10. ^ 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.
  11. ^ 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.
  12. ^ 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.
  13. ^ 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.
  14. ^ 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.
  15. ^ 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.
  16. ^ 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.
  17. ^ 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.
  18. ^ 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.
  19. ^ 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. doi:10.1128/AEM.01903-13. PMC 3811555. PMID 24014528.
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