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      Commensal bacteria and essential amino acids control food choice behavior and reproduction

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          Abstract

          Choosing the right nutrients to consume is essential to health and wellbeing across species. However, the factors that influence these decisions are poorly understood. This is particularly true for dietary proteins, which are important determinants of lifespan and reproduction. We show that in Drosophila melanogaster, essential amino acids (eAAs) and the concerted action of the commensal bacteria Acetobacter pomorum and Lactobacilli are critical modulators of food choice. Using a chemically defined diet, we show that the absence of any single eAA from the diet is sufficient to elicit specific appetites for amino acid (AA)-rich food. Furthermore, commensal bacteria buffer the animal from the lack of dietary eAAs: both increased yeast appetite and decreased reproduction induced by eAA deprivation are rescued by the presence of commensals. Surprisingly, these effects do not seem to be due to changes in AA titers, suggesting that gut bacteria act through a different mechanism to change behavior and reproduction. Thus, eAAs and commensal bacteria are potent modulators of feeding decisions and reproductive output. This demonstrates how the interaction of specific nutrients with the microbiome can shape behavioral decisions and life history traits.

          Author summary

          What animals, including humans, choose to eat has a tremendous impact on health and wellbeing. Though intake of dietary proteins and amino acids is essential for animals, excessive consumption of these nutrients is known to have detrimental effects. Many animals, therefore, execute precise control over the intake of these key nutrients. However, the factors controlling protein appetite are poorly understood. Here, we show that in the vinegar fly Drosophila melanogaster, essential amino acids and gut bacteria are key modulators of protein appetite. Lack of any one essential amino acid from the diet produces a strong and specific appetite for proteinaceous or amino acid–rich food. However, flies with an appropriate microbiome do not develop this protein appetite. Specifically, two gut bacteria species, Acetobacter pomorum and Lactobacilli, work together to suppress protein appetite. Furthermore, we show that flies lacking dietary essential amino acids have reduced reproductive output, an effect which is also rescued by gut bacteria. Finally, based on metabolite measurements, we propose that the influence of bacteria on host physiology and behavior is not mediated by changing amino acid levels. Our study demonstrates how the interaction of specific nutrients with the microbiome can shape behavior and animal fitness and suggests that they do so through a novel mechanism.

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          Most cited references58

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          Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera.

          A Douglas (1998)
          Most aphids possess intracellular bacteria of the genus Buchnera. The bacteria are transmitted vertically via the aphid ovary, and the association is obligate for both partners: Bacteria-free aphids grow poorly and produce few or no offspring, and Buchnera are both unknown apart from aphids and apparently unculturable. The symbiosis has a nutritional basis. Specifically, bacterial provisioning of essential amino acids has been demonstrated. Nitrogen recycling, however, is not quantitatively important to the nutrition of aphid species studied, and there is strong evidence against bacterial involvement in the lipid and sterol nutrition of aphids. Buchnera have been implicated in various non-nutritional functions. Of these, just one has strong experimental support: promotion of aphid transmission of circulative viruses. It is argued that strong parallels may exist between the nutritional interactions (including the underlying mechanisms) in the aphid-Buchnera association and other insect symbioses with intracellular microorganisms.
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            Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling.

            The symbiotic microbiota profoundly affect many aspects of host physiology; however, the molecular mechanisms underlying host-microbe cross-talk are largely unknown. Here, we show that the pyrroloquinoline quinone-dependent alcohol dehydrogenase (PQQ-ADH) activity of a commensal bacterium, Acetobacter pomorum, modulates insulin/insulin-like growth factor signaling (IIS) in Drosophila to regulate host homeostatic programs controlling developmental rate, body size, energy metabolism, and intestinal stem cell activity. Germ-free animals monoassociated with PQQ-ADH mutant bacteria displayed severe deregulation of developmental and metabolic homeostasis. Importantly, these defects were reversed by enhancing host IIS or by supplementing the diet with acetic acid, the metabolic product of PQQ-ADH.
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              Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing.

              There is growing evidence that intestinal bacteria are important beneficial partners of their metazoan hosts. Recent observations suggest a strong link between commensal bacteria, host energy metabolism, and metabolic diseases such as diabetes and obesity. As a consequence, the gut microbiota is now considered a "host" factor that influences energy uptake. However, the impact of intestinal bacteria on other systemic physiological parameters still remains unclear. Here, we demonstrate that Drosophila microbiota promotes larval growth upon nutrient scarcity. We reveal that Lactobacillus plantarum, a commensal bacterium of the Drosophila intestine, is sufficient on its own to recapitulate the natural microbiota growth-promoting effect. L. plantarum exerts its benefit by acting genetically upstream of the TOR-dependent host nutrient sensing system controlling hormonal growth signaling. Our results indicate that the intestinal microbiota should also be envisaged as a factor that influences the systemic growth of its host. Copyright © 2011 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: Writing – review & editing
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: ResourcesRole: Writing – review & editing
                Role: Resources
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                25 April 2017
                April 2017
                25 April 2017
                : 15
                : 4
                : e2000862
                Affiliations
                [1 ]Behavior and Metabolism Laboratory, Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Lisbon, Portugal
                [2 ]School of Biological Sciences, Monash University, Clayton, Victoria, Australia
                Rockefeller University, United States of America
                Author notes

                I have read the journal's policy and the authors of this manuscript have the following competing interests: PMI has a commercial interest in the flyPAD open-source technology.

                Author information
                http://orcid.org/0000-0002-9542-7335
                Article
                pbio.2000862
                10.1371/journal.pbio.2000862
                5404834
                28441450
                e6ff5c60-80e0-4200-bb24-e85de6d5d31d
                © 2017 Leitão-Gonçalves et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 18 August 2016
                : 15 March 2017
                Page count
                Figures: 7, Tables: 0, Pages: 29
                Funding
                Portuguese Foundation for Science and Technology (FCT) postdoctoral fellowship (grant number SFRH/BPD/78947/2011). Received by RLG. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Portuguese Foundation for Science and Technology (FCT) (grant number PTDC/BIA-BCM/118684/2010). Received by CR. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Human Frontier Science Program (grant number RGP0022/2012). Received by CR. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. EUROPEAN COMMISSION - MARIE CURIE ACTIONS FLiACT (grant number 289941). Received by CR. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Ciência sem Fronteiras program of the CNPq (grant number 200207/2012-1). Received by GTF. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Royal Society (grant number UF100158). Received by MDWP. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. BIAL Foundation (grant number 283/14). Received by CR. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. EMBO (grant number ALTF 1602-2011). Received by RLG. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Biotechnology and Biological Sciences Research Council (grant number BB/I011544/1). Received by MDWP. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Champalimaud Foundation. Received by CR. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Australian Research Council - Australian Research Council Future Fellow (grant number FT150100237). Received by MDWP. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Portuguese Foundation for Science and Technology (FCT) postdoctoral fellowship (grant number SFRH/BPD/76201/2011). Received by ZCS. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Portuguese Foundation for Science and Technology (FCT) postdoctoral fellowship (grant number SFRH/BPD/79325/2011). Received by PMI. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Kavli Foundation. Received by CR. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Physiology
                Physiological Processes
                Eating
                Appetite
                Medicine and Health Sciences
                Physiology
                Physiological Processes
                Eating
                Appetite
                Biology and Life Sciences
                Organisms
                Fungi
                Yeast
                Biology and Life Sciences
                Nutrition
                Nutrients
                Medicine and Health Sciences
                Nutrition
                Nutrients
                Biology and Life Sciences
                Nutrition
                Diet
                Medicine and Health Sciences
                Nutrition
                Diet
                Biology and Life Sciences
                Nutrition
                Diet
                Food
                Medicine and Health Sciences
                Nutrition
                Diet
                Food
                Biology and Life Sciences
                Organisms
                Bacteria
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbiome
                Biology and Life Sciences
                Genetics
                Genomics
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Microbiology
                Microbial Genomics
                Microbiome
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Carbohydrates
                Disaccharides
                Sucrose
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Carbohydrates
                Disaccharides
                Sucrose
                Custom metadata
                All relevant data have been uploaded as a Excel file to be published as a Supporting Information file.

                Life sciences
                Life sciences

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