The Drosophila Immune Deficiency Pathway Modulates Enteroendocrine Function and Host Metabolism

Kamareddine, Layla; Robins, William; Berkey, Cristin D.; Mekalanos, John J.; Watnick, Paula I.

doi:10.1016/j.cmet.2018.05.026

Cited by 134 publications

(165 citation statements)

References 52 publications

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“…Indeed, upon lactate utilization Acetobacter 630 may release molecules which would activate host endocrine signals and promote anabolism. Accordingly, it was recently shown that acetate produced by Acetobacter improves larval growth by impacting host lipid metabolism through the activation of the IMD signalling pathway in entero-endocrine cells and the release of the endocrine peptide tachykinin (Kamareddine et al, 2018). However, this mechanism is unlikely to 635 be at play here due to the high content of acetate in our fly diet.…”

Section: Lactate Utilization Also Triggers Another Major Class Of Metmentioning

confidence: 89%

Metabolic cooperation among commensal bacteria supportsDrosophilajuvenile growth under nutritional stress

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Grenier

Akherraz

et al. 2020

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SUMMARYThe gut microbiota shapes animal growth trajectory in stressful nutritional environments, but the molecular mechanisms behind such physiological benefits remain poorly understood. The gut microbiota is mostly composed of bacteria, which construct metabolic networks among themselves and with the host. Until now, how the metabolic activities of the microbiota contribute to host juvenile growth remains unknown. Here, using Drosophila as a host model, we report that two of its major bacterial partners, Lactobacillus plantarum and Acetobacter pomorum engage in a beneficial metabolic dialogue that boosts host juvenile growth despite nutritional stress. We pinpoint that lactate, produced by L. plantarum, is utilized by A. pomorum as an additional carbon source, and A. pomorum provides essential amino-acids and vitamins to L. plantarum. Such bacterial cross-feeding provisions a set of anabolic metabolites to the host, which may foster host systemic growth despite poor nutrition.GRAPHICAL ABSTRACTHIGHLIGHTSL. plantarum feeds lactate to A. pomorumA. pomorum supplies essential amino acids and vitamins to L. plantarumMicrobiota metabolic dialogue boosts Drosophila’s larval growthLactate utilization by Acetobacter releases anabolic metabolites to larvae

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Section: Lactate Utilization Also Triggers Another Major Class Of Metmentioning

confidence: 89%

Metabolic cooperation among commensal bacteria supportsDrosophilajuvenile growth under nutritional stress

Consuegra

Grenier

Akherraz

et al. 2020

Preprint

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“…Tachykinin-related peptide is a multifunctional neuropeptide, which may regulate insect immune system and metabolic homeostasis based on structure and functional homologs of vertebrate tachykinins (Urbanski and Rosinski, 2018). In D. melanogaster, intestinal microbiota and the microbial metabolite have also been found to activate innate immunity and promote the expression of the tachykinin-related peptide to promote host metabolic homeostasis (Kamareddine et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Neuropeptides and G-Protein Coupled Receptors (GPCRs) in the Red Palm Weevil Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae)

et al. 2020

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The red palm weevil Rhynchophorus ferrugineus is a devastating, invasive pest that causes serious damages to palm trees, and its invasiveness depends on its strong ability of physiological and behavioral adaptability. Neuropeptides and their receptors regulate physiology and behavior of insects, but these protein partners have not been identified from many insects. Here, we systematically identified neuropeptide precursors and the corresponding receptors in the red palm weevil, and analyzed their tissue expression patterns under control conditions and after pathogen infection. A total of 43 putative neuropeptide precursors were identified, including an extra myosuppressin peptide was identified with amino acid substitutions at two conserved sites. Forty-four putative neuropeptide receptors belonging to three classes were also identified, in which neuropeptide F receptors and insulin receptors were expanded compared to those in other insects. Based on qRT-PCR analyses, genes coding for several neuropeptide precursors and receptors were highly expressed in tissues other than the nervous system, suggesting that these neuropeptides and receptors play other roles in addition to neuro-reception. Some of the neuropeptides and receptors, like the tachykininrelated peptide and receptor, were significantly induced by pathogen infection, especially sensitive to Bacillus thuringiensis and Metarhizium anisopliae. Systemic identification and initial characterization of neuropeptides and their receptors in the red palm weevil provide a framework for further studies to reveal the functions of these ligand-and receptor-couples in regulating physiology, behavior, and immunity in this important insect pest species.

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“…Organisms harbor and interact with diverse microbial communities depending on their own ecology and environment. Furthermore, the microbiota are considered a fundamental aspect of a host's biology and are known to provide developmental cues, effect metabolism, and alter immunity [1][2][3], However, the microbiota constitutes a complex network of microorganisms and disentangling specific interactions at a mechanistic level is challenging. Bacterial-feeding nematodes therefore provide a highly attractive system to study the influence of the microbiota as the specific interactions can be investigated in monoxenic cultures where the microbiota and diet are indistinguishable from one another and easily controlled.…”

Section: Introductionmentioning

confidence: 99%

Bacterial vitamin B12 production enhances nematode predatory behavior

et al. 2020

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Although the microbiota is known to affect host development, metabolism, and immunity, its impact on host behavior is only beginning to be understood. In order to better characterize behavior modulation by host-associated microorganisms, we investigated how bacteria modulate complex behaviors in the nematode model organism Pristionchus pacificus. This nematode is a predator that feeds on the larvae of other nematodes, including Caenorhabditis elegans. By growing P. pacificus on different bacteria and testing their ability to kill C. elegans, we reveal large differences in killing efficiencies, with a Novosphingobium species showing the strongest enhancement. This enhanced killing was not accompanied by an increase in feeding, which is a phenomenon known as surplus killing, whereby predators kill more prey than necessary for sustenance. Our RNA-seq data demonstrate widespread metabolic rewiring upon exposure to Novosphingobium, which facilitated screening of bacterial mutants with altered transcriptional responses. We identified bacterial production of vitamin B 12 as an important cause of such enhanced predatory behavior. Although vitamin B 12 is an essential cofactor for detoxification and metabolite biosynthesis, shown previously to accelerate development in C. elegans, supplementation with this enzyme cofactor amplified surplus killing in P. pacificus, whereas mutants in vitamin B 12 -dependent pathways reduced surplus killing. By demonstrating that production of vitamin B 12 by hostassociated microbiota can affect complex host behaviors, we reveal new connections between animal diet, microbiota, and nervous system.

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The Drosophila Immune Deficiency Pathway Modulates Enteroendocrine Function and Host Metabolism

Cited by 134 publications

References 52 publications

Metabolic cooperation among commensal bacteria supportsDrosophilajuvenile growth under nutritional stress

Metabolic cooperation among commensal bacteria supportsDrosophilajuvenile growth under nutritional stress

Neuropeptides and G-Protein Coupled Receptors (GPCRs) in the Red Palm Weevil Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae)

Bacterial vitamin B12 production enhances nematode predatory behavior

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