Microbiome in the Drosophila gut

Short description: Microorganisms living in the fruit fly

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 links

## Microbial composition

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

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

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

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

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

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

1. ↑ "Microbiome interactions shape host fitness". Proceedings of the National Academy of Sciences of the United States of America 115 (51): E11951–E11960. December 2018. doi:10.1073/pnas.1809349115. PMID 30510004. Bibcode: 2018PNAS..11511951G.
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. PMID 34107298. PMC 8363570. http://dx.doi.org/10.1016/j.immuni.2021.05.017.
3. ↑ 3.0 3.1 3.2 3.3 3.4 "Host-intestinal microbiota mutualism: "learning on the fly"". Cell Host & Microbe 13 (1): 8–14. January 2013. doi:10.1016/j.chom.2012.12.004. PMID 23332152.
4. ↑ 4.0 4.1 "Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment". PLOS ONE 8 (8): e70749. 2013. doi:10.1371/journal.pone.0070749. PMID 23967097. Bibcode: 2013PLoSO...870749S.
5. ↑ "Gut-associated microbes of Drosophila melanogaster". Gut Microbes 3 (4): 307–21. 2012. doi:10.4161/gmic.19896. PMID 22572876.
6. ↑ "Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system". PLOS Genetics 7 (9): e1002272. September 2011. doi:10.1371/journal.pgen.1002272. PMID 21966276.
7. ↑ "Drosophila Perpetuates Nutritional Mutualism by Promoting the Fitness of Its Intestinal Symbiont Lactobacillus plantarum". Cell Metab. 27 (2): 362–377. February 2018. doi:10.1016/j.cmet.2017.11.011. PMID 29290388.
8. ↑ 8.0 8.1 "Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster". mBio 4 (6): e00860-13. November 2013. doi:10.1128/mbio.00860-13. PMID 24194543.
9. ↑ "The digestive tract of Drosophila melanogaster". Annual Review of Genetics 47: 377–404. 2013. doi:10.1146/annurev-genet-111212-133343. PMID 24016187. http://infoscience.epfl.ch/record/191313.
10. ↑ "Morphological and molecular characterization of adult midgut compartmentalization in Drosophila". Cell Reports 3 (5): 1725–38. May 2013. doi:10.1016/j.celrep.2013.04.001. PMID 23643535.
11. ↑ "Microbiota-induced changes in Drosophila melanogaster host gene expression and gut morphology". mBio 5 (3): e01117-14. May 2014. doi:10.1128/mbio.01117-14. PMID 24865556.
12. ↑ "Microbial Control of Intestinal Homeostasis via Enteroendocrine Cell Innate Immune Signaling". Trends in Microbiology 28 (2): 141–149. February 2020. doi:10.1016/j.tim.2019.09.005. PMID 31699645.
13. ↑ "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. August 2012. doi:10.1016/j.chom.2012.06.002. PMID 22901536.
14. ↑ "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. November 2010. doi:10.1073/pnas.1009906107. PMID 21041648.
15. ↑

* "Drosophila". Proceedings of the National Academy of Sciences of the United States of America 114 (48): 12767–12772. November 2017. doi:10.1073/pnas.1708345114. PMID 29109277.
* Miguel-Aliaga, Irene; Jasper, Heinrich; Lemaitre, Bruno (2018-10-01). "Anatomy and Physiology of the Digestive Tract of Drosophila melanogaster". Genetics (Genetics Society of America (OUP)) 210 (2): 357–396. doi:10.1534/genetics.118.300224. ISSN 1943-2631. PMID 30287514.
* 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. (AED ORCID: 0000-0001-5212-6826).
* "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. December 2018. 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 (The Company of Biologists) 224 (10). doi:10.1242/jeb.224485. ISSN 0022-0949. PMID 33988717.

16. ↑ "Drosophila lifespan enhancement by exogenous bacteria". Proceedings of the National Academy of Sciences of the United States of America 101 (35): 12974–9. August 2004. doi:10.1073/pnas.0405207101. PMID 15322271. Bibcode: 2004PNAS..10112974B.
17. ↑ "Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling". Science 334 (6056): 670–4. November 2011. doi:10.1126/science.1212782. PMID 22053049. Bibcode: 2011Sci...334..670S.
18. ↑ "Functional analysis of the Drosophila immune response during aging". Aging Cell 7 (2): 225–36. March 2008. doi:10.1111/j.1474-9726.2008.00370.x. PMID 18221416.
19. ↑ "Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila". Science 319 (5864): 777–82. February 2008. doi:10.1126/science.1149357. PMID 18218863. Bibcode: 2008Sci...319..777R.
20. ↑ "Noninvasive analysis of microbiome dynamics in the fruit fly Drosophila melanogaster". Applied and Environmental Microbiology 79 (22): 6984–8. November 2013. doi:10.1128/AEM.01903-13. PMID 24014528. Bibcode: 2013ApEnM..79.6984F.

## External links

* "Host-intestinal microbiota mutualism: "learning on the fly"". Cell Host & Microbe 13 (1): 8–14. January 2013. doi:10.1016/j.chom.2012.12.004. PMID 23332152.
* "Transient adult microbiota, gut homeostasis and longevity: novel insights from the Drosophila model". FEBS Letters 588 (22): 4250–7. November 2014. doi:10.1016/j.febslet.2014.06.041. PMID 24983497.
* "Noninvasive analysis of microbiome dynamics in the fruit fly Drosophila melanogaster". Applied and Environmental Microbiology 79 (22): 6984–8. November 2013. doi:10.1128/AEM.01903-13. PMID 24014528. Bibcode: 2013ApEnM..79.6984F.

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