Growth regulation by amino acid transporters in Drosophila larvae

Manière, Gérard; Alves, Georges; Berthelot-Grosjean, Martine; Grosjean, Yaël

doi:10.1007/s00018-020-03535-6

Cited by 28 publications

(22 citation statements)

References 59 publications

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“…In addition to micronutrients, amino acids are likely to impact host biology in different ways based on host-microbe, host-diet, and microbe-diet relationships ( 10 , 36 – 40 ). Our analysis showed that tryptophan was significantly increased with bacterial growth and, when administered in the diet to axenic flies, impacted fly life span.…”

Section: Discussionmentioning

confidence: 99%

Gut Bacteria Mediate Nutrient Availability in Drosophila Diets

Lesperance

Broderick

2020

Appl Environ Microbiol

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Drosophila melanogaster gut microbes play important roles in host nutritional physiology. However, these associations are often indirect and studies typically are in the context of specialized nutritional conditions, making it difficult to discern how microbiome-mediated impacts translate to physiologically relevant conditions, in the laboratory or nature. In this study, we quantified changes in dietary nutrients due to D. melanogaster gut bacteria on three artificial diets and a natural diet of grapes. We show that in all four diet conditions, bacteria altered protein, carbohydrates, and moisture of the food substrate. In depth analysis on one diet revealed that bacteria also increased tryptophan levels, an essential amino acid encountered scarcely in nature. These nutrient changes result in an increased protein to carbohydrate (P:C) ratio in all diets, which we hypothesized to be a significant determinant of microbiome-mediated host nutritional physiology. To test this, we compared life history traits of axenic flies reared on the three artificial diets with increased P:C or continuous bacterial inoculation. We found that, while on some diets an environment of nutritional plenitude had impacts on life history, it did not fully explain all microbiome-associated phenotypes. This suggests that other factors, such as micronutrients and feeding behavior, likely also contribute to life history traits in a diet-dependent manner. Thus, while some bacterial impacts on nutrition occur across diets, others are dictated by unique dietary environments, highlighting the importance of diet-microbiome interactions in D. melanogaster nutritional physiology. Importance Both in the laboratory and in nature, D. melanogaster-associated microbes serve as nutritional effectors, either through production of metabolites or as direct sources of protein biomass. The relationship between the microbiome and resulting host nutritional physiology is significantly impacted by diet composition, yet studies involving D. melanogaster are performed using a wide range of artificial diets, making it difficult to discern which aspects of host-microbe interactions may be universal or diet-dependent. In this study, we utilized three standard D. melanogaster diets and a natural grape diet to form a comprehensive understanding of the quantifiable nutritional changes mediated by the host microbial community. We then altered these artificial diets based on the observed microbe-mediated changes to demonstrate their potential to influence host physiology, allowing us to identify nutritional factors whose effects were either universal for the three artificial diets or dependent on host diet composition.

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Section: Discussionmentioning

confidence: 99%

Gut Bacteria Mediate Nutrient Availability in Drosophila Diets

Lesperance

Broderick

2020

Appl Environ Microbiol

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“…Indeed, the former acts in the fat body by sensing the amount free amino acids and remotely controls the secretion of Insulin Like Peptides (ILPs) by specialized cells located in the larval brain. The second is activated by circulating ILPs in peripheral tissues both to promote growth and to control duration of development (for review see [ 90 , 91 ] and references herein). Finally, we did not observe a decrease in food intake suggesting that spores and commercial products do not induce avoidance behavior.…”

Section: Discussionmentioning

confidence: 99%

Bacillus thuringiensis Bioinsecticides Induce Developmental Defects in Non-Target Drosophila melanogaster Larvae

Nawrot-Esposito

Babin

Pasco

et al. 2020

Insects

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Bioinsecticides made from the bacterium Bacillus thuringiensis (Bt) are the bestselling bioinsecticide worldwide. Among Bt bioinsecticides, those based on the strain Bt subsp. kurstaki (Btk) are widely used in farming to specifically control pest lepidopteran larvae. Although there is much evidence of the lack of acute lethality of Btk products for non-target animals, only scarce data are available on their potential non-lethal developmental adverse effects. Using a concentration that could be reached in the field upon sprayings, we show that Btk products impair growth and developmental time of the non-target dipteran Drosophila melanogaster. We demonstrate that these effects are mediated by the synergy between Btk bacteria and Btk insecticidal toxins. We further show that Btk bioinsecticides trigger intestinal cell death and alter protein digestion without modifying the food intake and feeding behavior of the larvae. Interestingly, these harmful effects can be mitigated by a protein-rich diet or by adding the probiotic bacterium Lactobacillus plantarum into the food. Finally, we unravel two new cellular mechanisms allowing the larval midgut to maintain its integrity upon Btk aggression: First the flattening of surviving enterocytes and second, the generation of new immature cells arising from the adult midgut precursor cells. Together, these mechanisms participate to quickly fill in the holes left by the dying enterocytes.

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“…Consistently, the protein level and release of Tk peptides in EEs are increased in starved flies and other insects to control gut mobility and EC lipogenesis (Winther and Nassel, 2001;Song et al, 2014), while refeeding flies only yeast that contains plenty of amino acids, but not sucrose or coconut oil, blunts the increase in Tk peptide level (Song et al, 2014). Several transporters or receptors that sense distinct amino acids and trigger the downstream signaling pathways have been characterized in Drosophila (Maniere et al, 2020). However, their roles in EEs are not fully identified yet.…”

Section: Amino Acidsmentioning

confidence: 96%

Physiological and Pathological Regulation of Peripheral Metabolism by Gut-Peptide Hormones in Drosophila

et al. 2020

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The gastrointestinal (GI) tract in both vertebrates and invertebrates is now recognized as a major source of signals modulating, via gut-peptide hormones, the metabolic activities of peripheral organs, and carbo-lipid balance. Key advances in the understanding of metabolic functions of gut-peptide hormones and their mediated interorgan communication have been made using Drosophila as a model organism, given its powerful genetic tools and conserved metabolic regulation. Here, we summarize recent studies exploring peptide hormones that are involved in the communication between the midgut and other peripheral organs/tissues during feeding conditions. We also highlight the emerging impacts of fly gut-peptide hormones on stress sensing and carbo-lipid metabolism in various disease models, such as energy overload, pathogen infection, and tumor progression. Due to the functional similarity of intestine and its derived peptide hormones between Drosophila and mammals, it can be anticipated that findings obtained in the fly system will have important implications for the understanding of human physiology and pathology.

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Growth regulation by amino acid transporters in Drosophila larvae

Cited by 28 publications

References 59 publications

Gut Bacteria Mediate Nutrient Availability in Drosophila Diets

Gut Bacteria Mediate Nutrient Availability in Drosophila Diets

Bacillus thuringiensis Bioinsecticides Induce Developmental Defects in Non-Target Drosophila melanogaster Larvae

Physiological and Pathological Regulation of Peripheral Metabolism by Gut-Peptide Hormones in Drosophila

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