Dietary Adaptation of Microbiota in Drosophila Requires NF-κB-Dependent Control of the Translational Regulator 4E-BP

Vandehoef, Crissie; Molaei, Maral; Karpac, Jason

doi:10.1016/j.celrep.2020.107736

Cited by 20 publications

(19 citation statements)

References 74 publications

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“…A recent study found nuclear factor-kB/Relish was vital to adapt gut microbiota species composition to host diet macronutrient composition, suggesting the importance of host genetic factors and diet components in shaping microbiota diversity (Vandehoef et al, 2020). The fecal bacteria of Fut2 − mice that lack fucosylated host glycans showed decreased alpha diversity relative to Fut2 + mice and exhibited significant differences in community composition (Kashyap et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Alteration and the Function of Intestinal Microbiota in High-Fat-Diet- or Genetics-Induced Lipid Accumulation

Qiao

Tan

et al. 2021

Front. Microbiol.

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Diet and host genetics influence the composition of intestinal microbiota, yet few studies have compared the function of intestinal microbiota in the diet- or genotype-induced lipid deposition, which limits our understanding of the role of intestinal bacteria in metabolic disorders. The lipid accumulation in wild-type zebrafish fed with control (CON) or high-fat (HF) diet and two gene-knockout zebrafish lines (cpt1b–/– or pparab–/–) fed with control diet was measured after a 4-week feeding experiment. The intestinal microbiota composition of these groups was investigated using 16S ribosomal RNA (rRNA) gene sequencing (DNA-based) and 16S rRNA sequencing (RNA-based). The HF diet or deficiency of two genes induced more weight gain and higher triglyceride content in the liver compared with their control group. 16S rRNA gene sequencing (DNA-based) indicated the decreased abundance of Proteobacteria in the HF group compared with CON, but there was no significant difference in bacterial α diversity among treatments. 16S rRNA sequencing (RNA-based) confirmed the decreased abundance of Proteobacteria and the bacterial α diversity in the HF group compared with CON. Deficiency of cpt1b or pparab showed less change in microbiota composition compared with their wild-type group. Intestinal microbiota of each group was transferred to germ-free zebrafish, and the quantification of Nile red staining indicated that the intestinal microbiota of the HF group induced more lipid accumulation compared with CON, whereas intestinal microbiota of cpt1b–/– and pparab–/– zebrafish did not. The results showed that RNA-based bacterial sequencing revealed more bacterial alteration than DNA-based bacterial sequencing. HF diet had a more dominant role in shaping gut microbiota composition to induce lipid accumulation compared with the gene-knockout of cpt1b or pparab in zebrafish, and the transplant of intestinal microbiota from HF-fed fish induced more lipid deposition in germ-free zebrafish. Together, these data suggested that a high-fat diet exerted a more dominant role over the deletion of cpt1b or pparab on the intestinal bacterial composition, which corresponded to lipid accumulation.

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Section: Discussionmentioning

confidence: 99%

Alteration and the Function of Intestinal Microbiota in High-Fat-Diet- or Genetics-Induced Lipid Accumulation

Qiao

Tan

et al. 2021

Front. Microbiol.

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“… D. melanogaster flies were surface sterilized with 70% ethanol and homogenized in 0.01 M phosphate-buffered saline (PBS) by using a motorized pestle. Homogenates were diluted up to 100-fold, plated onto LB agar, and then incubated aerobically at 37°C for 24 h. The characteristic colony morphology of BS168 was easily differentiated on LB, which is not a growth medium amenable to culturing the typical D. melanogaster microbiota ( 64 ).…”

Section: Methodsmentioning

confidence: 99%

Oxalate-Degrading Bacillus subtilis Mitigates Urolithiasis in a Drosophila melanogaster Model

Daisley

Chanyi

et al. 2020

mSphere

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Kidney stone disease is a morbid condition that is increasing in prevalence, with few nonsurgical treatment options. The majority of stones are composed of calcium oxalate. Unlike humans, some microbes can break down oxalate, suggesting that microbial therapeutics may provide a novel treatment for kidney stone patients. This study demonstrated that Bacillus subtilis 168 (BS168) decreased stone burden, improved health, and complemented the microbiota in a Drosophila melanogaster urolithiasis model, while not exacerbating calcium oxalate aggregation or adhesion to renal cells in vitro. These results identify this bacterium as a candidate for ameliorating stone formation; given that other strains of B. subtilis are components of fermented foods and are used as probiotics for digestive health, strain 168 warrants testing in humans. With the severe burden that recurrent kidney stone disease imposes on patients and the health care system, this microbial therapeutic approach could provide an inexpensive therapeutic adjunct.

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“…Drosophila harbors a simple gut microbiota composed of only a few dominant species, mainly belonging to Acetobacteraceae and Lactobacillaceae, which influence multiple aspects of fly physiology, such as growth (11,12), behavior (13), lifespan (14) and infection resistance (15,16). In turn, the microbiota can be shaped by various host and environmental factors such as food composition, or age of the flies (17)(18)(19)(20)(21).…”

Section: Introductionmentioning

confidence: 99%

Drosophilaantimicrobial peptides and lysozymes regulate gut microbiota composition and abundance

Marra

Hanson

Kondo

et al. 2021

Preprint

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The gut microbiota affects the physiology and metabolism of animals and its alteration can lead to diseases such as gut dysplasia or metabolic disorders. Several reports have shown that the immune system plays an important role in shaping both bacterial community composition and abundance in Drosophila, and that immune deficit, especially during aging, negatively affects microbiota richness and diversity. However, there has been little study at the effector level to demonstrate how immune pathways regulate the microbiota. A key set of Drosophila immune effectors are the antimicrobial peptides (AMPs), which confer defense upon systemic infection. AMPs and lysozymes, a group of digestive enzymes with antimicrobial properties, are expressed in the gut and are good candidates for microbiota regulation. Here, we take advantage of the model organism Drosophila melanogaster to investigate the role of AMPs and lysozymes in regulation of gut microbiota structure and diversity.Using flies lacking AMPs and newly generated lysozyme mutants, we colonized gnotobiotic flies with a defined set of commensal bacteria and analyzed changes in microbiota composition and abundance in vertical transmission and aging contexts through 16S rRNA gene amplicon sequencing. Our study shows that AMPs and, to a lesser extent, lysozymes are necessary to regulate the total and relative abundance of bacteria in the gut microbiota. We also decouple the direct function of AMPs from the IMD signaling pathway that regulates AMPs but also many other processes, more narrowly defining the role of these effectors in the microbial dysbiosis observed in IMD-deficient flies upon aging.ImportanceThis study advances current knowledge in the field of host-microbe interactions by demonstrating that the two families of immune effectors, antimicrobial peptides and lysozymes, actively regulate the gut microbiota composition and abundance. Consequences of the loss of these antimicrobial peptides and lysozymes are exacerbated during aging, and their loss contributes to increased microbiota abundance and shifted composition in old flies. This work shows that immune effectors, typically associated with resistance to pathogenic infections, also help shape the beneficial gut community, consistent with the idea that host-symbiont interactions use the same ‘language’ typically associated with pathogenesis.

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Dietary Adaptation of Microbiota in Drosophila Requires NF-κB-Dependent Control of the Translational Regulator 4E-BP

Abstract: Highlights d Midgut NF-kB/Relish function modulates dietary adaptation of microbiota d NF-kB/Relish limits the diet inducibility of 4E-BP/Thor d 4E-BP/Thor dictates diet-dependent changes in microbiota composition d Cap-dependent translation is required for dietary adaptation of microbiota

Cited by 20 publications

References 74 publications

Alteration and the Function of Intestinal Microbiota in High-Fat-Diet- or Genetics-Induced Lipid Accumulation

Alteration and the Function of Intestinal Microbiota in High-Fat-Diet- or Genetics-Induced Lipid Accumulation

Oxalate-Degrading Bacillus subtilis Mitigates Urolithiasis in a Drosophila melanogaster Model

Drosophilaantimicrobial peptides and lysozymes regulate gut microbiota composition and abundance

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