Microbes Promote Amino Acid Harvest to Rescue Undernutrition in Drosophila

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2015 Feb 17

PMID 25683709

Citations 85

Authors

Ryuichi Yamada

Sonali A Deshpande

Kimberley D Bruce

Elizabeth M Mak

William W Ja

Affiliations

Soon will be listed here.

Abstract

Microbes play an important role in the pathogenesis of nutritional disorders such as protein-specific malnutrition. However, the precise contribution of microbes to host energy balance during undernutrition is unclear. Here, we show that Issatchenkia orientalis, a fungal microbe isolated from field-caught Drosophila melanogaster, promotes amino acid harvest to rescue the lifespan of undernourished flies. Using radioisotope-labeled dietary components (amino acids, nucleotides, and sucrose) to quantify nutrient transfer from food to microbe to fly, we demonstrate that I. orientalis extracts amino acids directly from nutrient-poor diets and increases protein flux to the fly. This microbial association restores body mass, protein, glycerol, and ATP levels and phenocopies the metabolic profile of adequately fed flies. Our study uncovers amino acid harvest as a fundamental mechanism linking microbial and host metabolism, and highlights Drosophila as a platform for quantitative studies of host-microbe relationships.

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References

Prillinger H, Molnar O, Eliskases-Lechner F, Lopandic K . Phenotypic and genotypic identification of yeasts from cheese. Antonie Van Leeuwenhoek. 1999; 75(4):267-83. DOI: 10.1023/a:1001889917533. View

HADDAD S, LINDEGREN C . A method for determining the weight of an individual yeast cell. Appl Microbiol. 1953; 1(3):153-6. PMC: 1056888. DOI: 10.1128/am.1.3.153-156.1953. View

Brummel T, Ching A, Seroude L, Simon A, Benzer S . Drosophila lifespan enhancement by exogenous bacteria. Proc Natl Acad Sci U S A. 2004; 101(35):12974-9. PMC: 516503. DOI: 10.1073/pnas.0405207101. View

Murphy K, Teakle D, Macrae I . Kinetics of Colonization of Adult Queensland Fruit Flies (Bactrocera tryoni) by Dinitrogen-Fixing Alimentary Tract Bacteria. Appl Environ Microbiol. 1994; 60(7):2508-17. PMC: 201677. DOI: 10.1128/aem.60.7.2508-2517.1994. View

Carvalho G, Kapahi P, Anderson D, Benzer S . Allocrine modulation of feeding behavior by the Sex Peptide of Drosophila. Curr Biol. 2006; 16(7):692-6. PMC: 2745344. DOI: 10.1016/j.cub.2006.02.064. View

Turnbaugh P, Ley R, Mahowald M, Magrini V, Mardis E, Gordon J . An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006; 444(7122):1027-31. DOI: 10.1038/nature05414. View

Ja W, Carvalho G, Mak E, de la Rosa N, Fang A, Liong J . Prandiology of Drosophila and the CAFE assay. Proc Natl Acad Sci U S A. 2007; 104(20):8253-6. PMC: 1899109. DOI: 10.1073/pnas.0702726104. View

Ley R, Hamady M, Lozupone C, Turnbaugh P, Ramey R, Bircher J . Evolution of mammals and their gut microbes. Science. 2008; 320(5883):1647-51. PMC: 2649005. DOI: 10.1126/science.1155725. View

Turnbaugh P, Hamady M, Yatsunenko T, Cantarel B, Duncan A, Ley R . A core gut microbiome in obese and lean twins. Nature. 2008; 457(7228):480-4. PMC: 2677729. DOI: 10.1038/nature07540. View

10.

Daniel H, Vrancken G, Takrama J, Camu N, de Vos P, De Vuyst L . Yeast diversity of Ghanaian cocoa bean heap fermentations. FEMS Yeast Res. 2009; 9(5):774-83. DOI: 10.1111/j.1567-1364.2009.00520.x. View

11.

Wilfrid Padonou S, Nielsen D, Hounhouigan J, Thorsen L, Nago M, Jakobsen M . The microbiota of Lafun, an African traditional cassava food product. Int J Food Microbiol. 2009; 133(1-2):22-30. DOI: 10.1016/j.ijfoodmicro.2009.04.019. View

12.

Zid B, Rogers A, Katewa S, Vargas M, Kolipinski M, Lu T . 4E-BP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila. Cell. 2009; 139(1):149-60. PMC: 2759400. DOI: 10.1016/j.cell.2009.07.034. View

13.

Chavan P, Mane S, Kulkarni G, Shaikh S, Ghormade V, Nerkar D . Natural yeast flora of different varieties of grapes used for wine making in India. Food Microbiol. 2009; 26(8):801-8. DOI: 10.1016/j.fm.2009.05.005. View

14.

Ja W, Carvalho G, Zid B, Mak E, Brummel T, Benzer S . Water- and nutrient-dependent effects of dietary restriction on Drosophila lifespan. Proc Natl Acad Sci U S A. 2009; 106(44):18633-7. PMC: 2773996. DOI: 10.1073/pnas.0908016106. View

15.

Claesson M, Cusack S, OSullivan O, Greene-Diniz R, de Weerd H, Flannery E . Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci U S A. 2010; 108 Suppl 1:4586-91. PMC: 3063589. DOI: 10.1073/pnas.1000097107. View

16.

Dethlefsen L, Relman D . Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci U S A. 2010; 108 Suppl 1:4554-61. PMC: 3063582. DOI: 10.1073/pnas.1000087107. View

17.

Jumpertz R, Le D, Turnbaugh P, Trinidad C, Bogardus C, Gordon J . Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am J Clin Nutr. 2011; 94(1):58-65. PMC: 3127503. DOI: 10.3945/ajcn.110.010132. View

18.

Wong C, Ng P, Douglas A . Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environ Microbiol. 2011; 13(7):1889-900. PMC: 3495270. DOI: 10.1111/j.1462-2920.2011.02511.x. View

19.

Yang J, Nam H, Seo M, Han S, Choi Y, Nam H . OASIS: online application for the survival analysis of lifespan assays performed in aging research. PLoS One. 2011; 6(8):e23525. PMC: 3156233. DOI: 10.1371/journal.pone.0023525. View

20.

Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F . Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab. 2011; 14(3):403-14. DOI: 10.1016/j.cmet.2011.07.012. View