Cited by 315Neurobiology and Insect Physiology ResearchInsect symbiosis and bacterial influencesGut microbiota and health

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

Open access
Leitão-Gonçalves, Ricardo, Carvalho-Santos, Zita, Francisco, Ana Patrícia, Fioreze, Gabriela Tondolo, Anjos, Margarida, Baltazar, Célia, Elias, Ana Paula, Itskov, Pavel M. +2 more·2017·PLOS Biology

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pbio.2000862

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • In Drosophila, giving GF flies Acetobacter pomorum and Lactobacillus spp. changed their overall food preference.

    “However, an intriguing study in Drosophila points to a key role for the microbiota in food choice behavior, as when GF flies were given Acetobacter pomorum and Lactobacillus spp., it changed their overall food preference (Leitao-Goncalves et al., 2017).”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Leitao-Goncalves et al., 2017

    The Results section, “Acetobacter pomorum acts together with Lactobacilli to modify food choice” (page unavailable), reports that adding A. pomorum with either L. plantarum or L. brevis suppressed yeast appetite in essential-amino-acid-deprived flies. The Methods confirm that these experiments used axenic or gnotobiotic flies. The claim’s “overall food preference” is broader than the specific, deprivation-dependent yeast preference the paper tested. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 96 · Cited by 315

Research works printed but not linked: 82

  1. [2]Simpson SJ, Raubenheimer D. The nature of nutrition. Princeton, Princeton University Press; 2012.
  2. [3]Simpson SJ, Le Couteur DG, Raubenheimer D. Putting the Balance Back in Diet. Cell. 2015; 161: 18– 23. 10.1016/j.cell.2015.02.033 25815981 · DOI
  3. [4]Levine ME, Suarez JA, Brandhorst S, Balasubramanian P, Cheng C-W, Madia F, et al Low Protein Intake Is Associated with a Major Reduction in IGF-1, Cancer, and Overall Mortality in the 65 and Younger but Not Older Population. Cell Metab. 2014; 19: 407– 417. 10.1016/j.cmet.2014.02.006 24606898 PMC3988204 · DOI · Paper page
  4. [6]Lee KP, Simpson SJ, Clissold FJ, Brooks R, Ballard JWO, Taylor PW, et al Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proc Natl Acad Sci. 2008; 105: 2498– 2503. 10.1073/pnas.0710787105 18268352 PMC2268165 · DOI · Paper page
  5. [7]Piper MDW, Blanc E, Leitão-Gonçalves R, Yang M, He X, Linford NJ, et al A holidic medium for Drosophila melanogaster. Nat Methods. 2013; 11: 100– 105. 10.1038/nmeth.2731 24240321 PMC3877687 · DOI
  6. [8]Piper MDW, Partridge L, Raubenheimer D, Simpson SJ. Dietary Restriction and Aging: A Unifying Perspective. Cell Metab. 2011; 14: 154– 160. 10.1016/j.cmet.2011.06.013 21803286 PMC4445606 · DOI
  7. [9]Grandison RC, Piper MDW, Partridge L. Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature. 2009; 462: 1061– 1064. 10.1038/nature08619 19956092 PMC2798000 · DOI
  8. [10]Gosby AK, Conigrave AD, Lau NS, Iglesias MA, Hall RM, Jebb SA, et al Testing Protein Leverage in Lean Humans: A Randomised Controlled Experimental Study. Morrison C, editor. PLoS ONE. 2011; 6: e25929 10.1371/journal.pone.0025929 22022472 PMC3192127 · DOI
  9. [11]Griffioen-Roose S, Mars M, Siebelink E, Finlayson G, Tome D, de Graaf C. Protein status elicits compensatory changes in food intake and food preferences. Am J Clin Nutr. 2012; 95: 32– 38. 10.3945/ajcn.111.020503 22158729 PMC3238463 · DOI · Paper page
  10. [12]Ribeiro C, Dickson BJ. Sex Peptide Receptor and Neuronal TOR/S6K Signaling Modulate Nutrient Balancing in Drosophila. Curr Biol. 2010; 20: 1000– 1005. 10.1016/j.cub.2010.03.061 20471268 · DOI
  11. [13]Itskov PM, Ribeiro C. The Dilemmas of the Gourmet Fly: The Molecular and Neuronal Mechanisms of Feeding and Nutrient Decision Making in Drosophila. Front Neurosci. 2013; 7: 12 10.3389/fnins.2013.00012 23407678 PMC3569668 · DOI
  12. [14]Walker SJ, Corrales-Carvajal VM, Ribeiro C. Postmating Circuitry Modulates Salt Taste Processing to Increase Reproductive Output in Drosophila. Curr Biol. 2015; 25: 2621– 2630. 10.1016/j.cub.2015.08.043 26412135 · DOI
  13. [15]Vargas MA, Luo N, Yamaguchi A, Kapahi P. A Role for S6 Kinase and Serotonin in Postmating Dietary Switch and Balance of Nutrients in D. melanogaster. Curr Biol. 2010; 20: 1006– 1011. 10.1016/j.cub.2010.04.009 20471266 PMC2885474 · DOI
  14. [16]Corrales-Carvajal VM, Faisal AA, Ribeiro C. Internal states drive nutrient homeostasis by modulating exploration-exploitation trade-off. eLife. 2016; 5: e19920 10.7554/eLife.19920 27770569 PMC5108593 · DOI
  15. [18]Bos M, Burnet B, Farrow R, Woods RA. Development of Drosophila on sterol mutants of the yeast Saccharomyces cerevisiae. Genet Res. 1976; 28: 163– 176. 795728
  16. [19]Subramanian S, Blanton LV, Frese SA, Charbonneau M, Mills DA, Gordon JI. Cultivating Healthy Growth and Nutrition through the Gut Microbiota. Cell. 2015; 161: 36– 48. 10.1016/j.cell.2015.03.013 25815983 PMC4440586 · DOI
  17. [20]Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome, and immune system: envisioning the future. Nature. 2011; 474: 327– 336. 10.1038/nature10213 21677749 PMC3298082 · DOI · Paper page
  18. [21]Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006; 444: 1027– 131. 10.1038/nature05414 17183312 · DOI · Paper page
  19. [25]Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012; 13: 701– 712. 10.1038/nrn3346 22968153 · DOI · Paper page
  20. [26]Mayer EA, Knight R, Mazmanian SK, Cryan JF, Tillisch K. Gut Microbes and the Brain: Paradigm Shift in Neuroscience. J Neurosci. 2014; 34: 15490– 15496. 10.1523/JNEUROSCI.3299-14.2014 25392516 PMC4228144 · DOI · Paper page
  21. [27]Sampson TR, Mazmanian SK. Control of Brain Development, Function, and Behavior by the Microbiome. Cell Host Microbe. 2015; 17: 565– 576. 10.1016/j.chom.2015.04.011 25974299 PMC4442490 · DOI · Paper page
  22. [28]Ezenwa VO, Gerardo NM, Inouye DW, Medina M, Xavier JB. Animal Behavior and the Microbiome. Science. 2012; 338: 198– 199. 10.1126/science.1227412 23066064 · DOI
  23. [30]Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, Srinivasan S, et al Metabolic Syndrome and Altered Gut Microbiota in Mice Lacking Toll-Like Receptor 5. Science. 2010; 328: 228– 231. 10.1126/science.1179721 20203013 PMC4714868 · DOI · Paper page
  24. [33]Neufeld KM, Kang N, Bienenstock J, Foster JA. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil. 2011; 23: 255– e119. 10.1111/j.1365-2982.2010.01620.x 21054680 · DOI · Paper page
  25. [34]Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, et al Microbiota Modulate Behavioral and Physiological Abnormalities Associated with Neurodevelopmental Disorders. Cell. 2013; 155: 1451– 1463. 10.1016/j.cell.2013.11.024 24315484 PMC3897394 · DOI · Paper page
  26. [35]Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci. 2010; 107: 20051– 20056. 10.1073/pnas.1009906107 21041648 PMC2993361 · DOI
  27. [36]Huang J-H, Douglas AE. Consumption of dietary sugar by gut bacteria determines Drosophila lipid content. Biol Lett. 2015; 11: 20150469 10.1098/rsbl.2015.0469 26382071 PMC4614424 · DOI
  28. [37]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: 403– 414. 10.1016/j.cmet.2011.07.012 21907145 · DOI
  29. [38]Shin SC, Kim S-H, You H, Kim B, Kim AC, Lee K-A, et al Drosophila Microbiome Modulates Host Developmental and Metabolic Homeostasis via Insulin Signaling. Science. 2011; 334: 670– 674. 10.1126/science.1212782 22053049 · DOI
  30. [39]Schwarzer M, Makki K, Storelli G, Machuca-Gayet I, Srutkova D, Hermanova P, et al Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science. 2016; 351: 854– 857. 10.1126/science.aad8588 26912894 · DOI
  31. [41]Tanimura T, Isono K, Takamura T, Shimada I. Genetic dimorphism in the taste sensitivity to trehalose in Drosophila melanogaster. J Comp Physiol. 1982; 147: 433– 437.
  32. [42]Toshima N, Tanimura T. Taste preference for amino acids is dependent on internal nutritional state in Drosophila melanogaster. J Exp Biol. 2012; 215: 2827– 2832. 10.1242/jeb.069146 22837455 · DOI
  33. [43]Bender DA. Amino Acid Metabolism. John Wiley & Sons; 2012.
  34. [44]Wu G, Wu Z, Dai Z, Yang Y, Wang W, Liu C, et al Dietary requirements of “nutritionally non-essential amino acids” by animals and humans. Amino Acids. 2012; 44: 1107– 1113. 10.1007/s00726-012-1444-2 23247926 · DOI
  35. [45]Simpson CL, Simpson SJ, Abisgold JD. The role of various amino acids in the protein compensatory response of locusta migratoria. Symposia Biologica Hungarica 1991; 39: 39– 46.
  36. [46]Hara K, Yonezawa K, Weng Q-P, Kozlowski MT, Belham C, Avruch J. Amino Acid Sufficiency and mTOR Regulate p70 S6 Kinase and eIF-4E BP1 through a Common Effector Mechanism. J Biol Chem. 1998; 273: 14484– 14494. 9603962
  37. [47]Ja WW, Carvalho GB, Mak EM, de la Rosa NN, Fang AY, Liong JC, et al Prandiology of Drosophila and the CAFE assay. Proc Natl Acad Sci. 2007; 104: 8253– 8256. 10.1073/pnas.0702726104 17494737 PMC1899109 · DOI
  38. [48]Silva FJ, Bel Y, Botella LM, Cotton RGH, Ferré J. Immunological detection of phenylalanine hydroxylase protein in Drosophila melanogaster. Biochem J. 1992; 287: 85– 89. 1417795 PMC1133127
  39. [49]Fölling A. Über Ausscheidung von Phenylbrenztraubensäure in den Harn als Stoffwechselanomalie in Verbindung mit Imbezillität. Hoppe-Seyler´s Z Für Physiol Chem. 1934; 227: 169– 181.
  40. [50]Mitchell JJ, Trakadis YJ, Scriver CR. Phenylalanine hydroxylase deficiency. Genet Med Off J Am Coll Med Genet. 2011; 13: 697– 707. 21555948
  41. [51]de Groot MJ, Hoeksma M, Blau N, Reijngoud DJ, van Spronsen FJ. Pathogenesis of cognitive dysfunction in phenylketonuria: Review of hypotheses. Mol Genet Metab. 2010; 99, Supplement: S86– S89. 20123477
  42. [52]MacDonald A, Rocha JC, van Rijn M, Feillet F. Nutrition in phenylketonuria. Mol Genet Metab. 2011; 104: S10– S18. 10.1016/j.ymgme.2011.08.023 21944460 · DOI
  43. [53]Vajro P, Strisciuglio P, Houssin D, Huault G, Laurent J, Alvarez F, et al Correction of Phenylketonuria after Liver Transplantation in a Child with Cirrhosis. N Engl J Med. 1993; 329: 363– 363. 8321274
  44. [54]Udenfriend S, Cooper JR. The enzymatic conversion of phenylalanine to tyrosine. J Biol Chem. 1952; 194: 503– 511. 14927641
  45. [55]Kilby BA, Neville E. Amino-acid metabolism in locust tissues. J Exp Biol. 1957; 34: 276– 289. 13315294
  46. [56]Arrese EL, Soulages JL. Insect Fat Body: Energy, Metabolism, and Regulation. Annu Rev Entomol. 2010; 55: 207– 225. 10.1146/annurev-ento-112408-085356 19725772 PMC3075550 · DOI
  47. [57]Neckameyer WS, Coleman CM, Eadie S, Goodwin SF. Compartmentalization of neuronal and peripheral serotonin synthesis in Drosophila melanogaster. Genes Brain Behav. 2007; 6: 756– 769. 10.1111/j.1601-183X.2007.00307.x 17376153 · DOI
  48. [58]Schmid MR, Anderl I, Vesala L, Vanha-aho L-M, Deng X-J, Rämet M, et al Control of Drosophila Blood Cell Activation via Toll Signaling in the Fat Body. PLoS ONE. 2014; 9: e102568 10.1371/journal.pone.0102568 25102059 PMC4125153 · DOI
  49. [59]Hacquard S, Garrido-Oter R, González A, Spaepen S, Ackermann G, Lebeis S, et al Microbiota and Host Nutrition across Plant and Animal Kingdoms. Cell Host Microbe. 2015; 17: 603– 616. 10.1016/j.chom.2015.04.009 25974302 · DOI · Paper page
  50. [60]Wong AC-N, Dobson AJ, Douglas AE. Gut microbiota dictates the metabolic response of Drosophila to diet. J Exp Biol. 2014; 217: 1894– 1901. 10.1242/jeb.101725 24577449 PMC4037322 · DOI
  51. [61]Blum JE, Fischer CN, Miles J, Handelsman J. Frequent Replenishment Sustains the Beneficial Microbiome of Drosophila melanogaster. mBio. 2013; 4: e00860– 13. 10.1128/mBio.00860-13 24194543 PMC3892787 · DOI
  52. [62]Ryu J-H, Kim S-H, Lee H-Y, Bai JY, Nam Y-D, Bae J-W, et al Innate Immune Homeostasis by the Homeobox Gene Caudal and Commensal-Gut Mutualism in Drosophila. Science. 2008; 319: 777– 782. 10.1126/science.1149357 18218863 · DOI
  53. [63]Cox CR, Gilmore MS. Native Microbial Colonization of Drosophila melanogaster and Its Use as a Model of Enterococcus faecalis Pathogenesis. Infect Immun. 2007; 75: 1565– 1576. 10.1128/IAI.01496-06 17220307 PMC1865669 · DOI
  54. [64]Hansen IA, Attardo GM, Park J-H, Peng Q, Raikhel AS. Target of rapamycin-mediated amino acid signaling in mosquito anautogeny. Proc Natl Acad Sci U S A. 2004; 101: 10626– 10631. 10.1073/pnas.0403460101 15229322 PMC489984 · DOI
  55. [65]Drummond-Barbosa D, Spradling AC. Stem Cells and Their Progeny Respond to Nutritional Changes during Drosophila Oogenesis. Dev Biol. 2001; 231: 265– 278. 10.1006/dbio.2000.0135 11180967 · DOI
  56. [66]Hosios AM, Hecht VC, Danai LV, Johnson MO, Rathmell JC, Steinhauser ML, et al Amino Acids Rather than Glucose Account for the Majority of Cell Mass in Proliferating Mammalian Cells. Dev Cell. 2016; 36: 540– 549. 10.1016/j.devcel.2016.02.012 26954548 PMC4766004 · DOI · Paper page
  57. [67]Itskov PM, Moreira J-M, Vinnik E, Lopes G, Safarik S, Dickinson MH, et al Automated monitoring and quantitative analysis of feeding behaviour in Drosophila. Nat Commun. 2014; 5: 4560 10.1038/ncomms5560 25087594 PMC4143931 · DOI
  58. [68]Newell PD, Douglas AE. Interspecies Interactions Determine the Impact of the Gut Microbiota on Nutrient Allocation in Drosophila melanogaster. Appl Environ Microbiol. 2014; 80: 788– 796. 10.1128/AEM.02742-13 24242251 PMC3911109 · DOI
  59. [69]Douglas AE. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol. 1998; 43: 17– 37. 10.1146/annurev.ento.43.1.17 15012383 · DOI
  60. [70]Bjordal M, Arquier N, Kniazeff J, Pin JP, Léopold P. Sensing of Amino Acids in a Dopaminergic Circuitry Promotes Rejection of an Incomplete Diet in Drosophila. Cell. 2014; 156: 510– 521. 10.1016/j.cell.2013.12.024 24485457 · DOI
  61. [71]Hao S. Uncharged tRNA and Sensing of Amino Acid Deficiency in Mammalian Piriform Cortex. Science. 2005; 307: 1776– 1778. 10.1126/science.1104882 15774759 · DOI
  62. [72]Maurin A-C, Jousse C, Averous J, Parry L, Bruhat A, Cherasse Y, et al The GCN2 kinase biases feeding behavior to maintain amino acid homeostasis in omnivores. Cell Metab. 2005; 1: 273– 277. 10.1016/j.cmet.2005.03.004 16054071 · DOI
  63. [73]Leib DE, Knight ZA. Re-examination of Dietary Amino Acid Sensing Reveals a GCN2-Independent Mechanism. Cell Rep. 2015; 13: 1081– 1089. 10.1016/j.celrep.2015.09.055 26526991 PMC4836942 · DOI
  64. [74]Simpson SJ, Simpson CL. Mechanisms Controlling Modulation by Haemolymph Amino Acids of Gustatory Responsiveness in the Locust. J Exp Biol. 1992; 168: 269– 287.
  65. [75]Brummel T, Ching A, Seroude L, Simon AF, Benzer S. Drosophila lifespan enhancement by exogenous bacteria. Proc Natl Acad Sci U S A. 2004; 101: 12974– 12979. 10.1073/pnas.0405207101 15322271 PMC516503 · DOI
  66. [76]Elgart M, Stern S, Salton O, Gnainsky Y, Heifetz Y, Soen Y. Impact of gut microbiota on the fly’s germ line. Nat Commun. 2016; 7: 11280 10.1038/ncomms11280 27080728 PMC4835552 · DOI
  67. [77]Yamada R, Deshpande SA, Bruce KD, Mak EM, Ja WW. Microbes Promote Amino Acid Harvest to Rescue Undernutrition in Drosophila. Cell Rep. 2015; 10: 865– 872. PMC4534362 25683709
  68. [78]Erkosar B, Storelli G, Mitchell M, Bozonnet L, Bozonnet N, Leulier F. Pathogen Virulence Impedes Mutualist-Mediated Enhancement of Host Juvenile Growth via Inhibition of Protein Digestion. Cell Host Microbe. 2015; 18: 445– 455. 10.1016/j.chom.2015.09.001 26439865 PMC4617634 · DOI
  69. [80]Attardo GM, Higgs S, Klingler KA, Vanlandingham DL, Raikhel AS. RNA interference-mediated knockdown of a GATA factor reveals a link to anautogeny in the mosquito Aedes aegypti. Proc Natl Acad Sci. 2003; 100: 13374– 13379. 10.1073/pnas.2235649100 14595016 PMC263821 · DOI
  70. [81]Arsic D, Guerin PM. Nutrient content of diet affects the signaling activity of the insulin/target of rapamycin/p70 S6 kinase pathway in the African malaria mosquito Anopheles gambiae. J Insect Physiol. 2008; 54: 1226– 1235. 10.1016/j.jinsphys.2008.06.003 18634792 · DOI
  71. [82]Ables ET, Laws KM, Drummond-Barbosa D. Control of adult stem cells in vivo by a dynamic physiological environment: diet-dependent systemic factors in Drosophila and beyond. Wiley Interdiscip Rev Dev Biol. 2012; 1: 657– 674. 10.1002/wdev.48 23799567 PMC3733242 · DOI
  72. [83]LaFever L, Feoktistov A, Hsu H-J, Drummond-Barbosa D. Specific roles of Target of rapamycin in the control of stem cells and their progeny in the Drosophila ovary. Development. 2010; 137: 2117– 2126. 10.1242/dev.050351 20504961 PMC2882131 · DOI
  73. [84]Theis KR, Dheilly NM, Klassen JL, Brucker RM, Baines JF, Bosch TCG, et al Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes. mSystems. 2016; 1: e00028– 16. PMC5069740 27822520
  74. [85]Erkosar B, Storelli G, Defaye A, Leulier F. Host-Intestinal Microbiota Mutualism: “Learning on the Fly.” Cell Host Microbe. 2013; 13: 8– 14. 10.1016/j.chom.2012.12.004 23332152 · DOI
  75. [86]Lee W-J, Brey PT. How Microbiomes Influence Metazoan Development:Insights from History and Drosophila Modeling of Gut-Microbe Interactions. Annu Rev Cell Dev Biol. 2013; 29: 571– 592. 10.1146/annurev-cellbio-101512-122333 23808845 · DOI
  76. [88]Tărlungeanu DC, Deliu E, Dotter CP, Kara M, Janiesch PC, Scalise M, et al Impaired Amino Acid Transport at the Blood Brain Barrier Is a Cause of Autism Spectrum Disorder. Cell. 2016; 167: 1481– 1494.e18. 10.1016/j.cell.2016.11.013 27912058 PMC5554935 · DOI · Paper page
  77. [89]Lee T, Luo L. Mosaic Analysis with a Repressible Cell Marker for Studies of Gene Function in Neuronal Morphogenesis. Neuron. 1999; 22: 451– 461. 10197526
  78. [90]Luo L, Liao YJ, Jan LY, Jan YN. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 1994; 8: 1787– 1802. 7958857
  79. [91]Förster D, Luschnig S. Src42A-dependent polarized cell shape changes mediate epithelial tube elongation in Drosophila. Nat Cell Biol. 2012; 14: 526– 534. 10.1038/ncb2456 22446736 · DOI
  80. [92]Asha H, Nagy I, Kovacs G, Stetson D, Ando I, Dearolf CR. Analysis of Ras-Induced Overproliferation in Drosophila Hemocytes. Genetics. 2003; 163: 203– 215. 12586708 PMC1462399
  81. [93]Piper MD, Soultoukis GA, Blanc E, Mesaros A, Herbert SL, Juridic P, et al Matching Dietary Amino Acid Balance to the In Silico Translated Exome Optimizes Growth and Reproduction without Cost to Lifespan. Cell Metab. 2017; 25: 610– 621. 10.1016/j.cmet.2017.02.005 28273481 PMC5355364 · DOI
  82. [94]Wayland MT, Defaye A, Rocha J, Jayaram SA, Royet J, Miguel-Aliaga I, et al Spotting the differences: Probing host/microbiota interactions with a dedicated software tool for the analysis of faecal outputs in Drosophila. J Insect Physiol. 2014; 69: 126– 135. 10.1016/j.jinsphys.2014.05.023 24907675 PMC4194350 · DOI

Authors
Leitão-Gonçalves, R., Carvalho-Santos, Z., Francisco, A. P., Fioreze, G. T., Anjos, M., Baltazar, C., Elias, A. P., Itskov, P. M., Piper, M. D. W., & Ribeiro, C.
Affiliations
  • Centro Champalimaud (PT)
  • Monash University (AU)
Corresponding author
Ribeiro, Carlos
Venue
PLOS Biology
Published
2017-04-25
Volume
15
Issue
4
Pages
e2000862
ISSN
  • 1544-9173 (ISSN-L)
  • 1545-7885
OpenAlex
W2608401495
Cited by
315
References
96
Citations by year
2026: 27 · 2025: 28 · 2024: 25 · 2023: 37 · 2022: 28 · 2021: 39 · 2020: 45 · 2019: 36 · 2018: 35 · 2017: 15
FWCI
17.54
Type
journal article
Language
en
Open access
Locations
  • PLoS Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Monash University Research Portal (Monash University) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • European Commission (289941)
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico
  • Fundação Bial
  • Fundação Champalimaud
  • National Institutes of Health (NIH P40OD018537, P40OD018537)
  • Directorate for Biological Sciences
  • Biotechnology and Biological Sciences Research Council (BB/I011544/1)
  • Australian Research Council (FT150100237)
  • Fundação para a Ciência e a Tecnologia (SFRH/BPD/78947/2011, PTDC/BIA-BCM/118684/2010, SFRH/BPD/76201/2011)
  • Ciência sem Fronteiras
  • Institute of Genetics
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect symbiosis and bacterial influences
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords
commensal bacteria, essential amino acids, food choice, Drosophila melanogaster, Acetobacter pomorum, lactobacilli, amino acid starvation, reproduction, gut microbiota, nutrient sensing, feeding behavior, life-history traits
MeSH terms
Gastrointestinal Microbiome, Acetobacter, Amino Acids, Essential, Animals, Appetite Regulation, Behavior, Animal, Drosophila melanogaster, Feeding Behavior, Female, Food Preferences, Host-Parasite Interactions, Lactobacillus, Oviposition, Species Specificity, Enterococcus faecalis, Symbiosis, Yeast, Dried, Acetobacteraceae, Drosophila Proteins, Animals, Genetically Modified, Complex Mixtures, Gene Knockout Techniques

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review