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Host Species and Environmental Effects on Bacterial Communities Associated with Drosophila in the Laboratory and in the Natural Environment

Fabian Staubach, John F. Baines, Sven Künzel and 2 more

PLoS ONE · 2013

doi:10.1371/journal.pone.0070749

Abstract

The fruit fly Drosophila is a classic model organism to study adaptation as well as the relationship between genetic variation and phenotypes. Although associated bacterial communities might be important for many aspects of Drosophila biology, knowledge about their diversity, composition, and factors shaping them is limited. We used 454-based sequencing of a variable region of the bacterial 16S ribosomal RNA gene to characterize the bacterial communities associated with wild and laboratory Drosophila isolates. In order to specifically investigate effects of food source and host species on bacterial communities, we analyzed samples from wild Drosophila melanogaster and D. simulans collected from a variety of natural substrates, as well as from adults and larvae of nine laboratory-reared Drosophila species. We find no evidence for host species effects in lab-reared flies; instead, lab of origin and stochastic effects, which could influence studies of Drosophila phenotypes, are pronounced. In contrast, the natural Drosophila-associated microbiota appears to be predominantly shaped by food substrate with an additional but smaller effect of host species identity. We identify a core member of this natural microbiota that belongs to the genus Gluconobacter and is common to all wild-caught flies in this study, but absent from the laboratory. This makes it a strong candidate for being part of what could be a natural D. melanogaster and D. simulans core microbiome. Furthermore, we were able to identify candidate pathogens in natural fly isolates.

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References 59

  1. 1.

    Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, et al (2012 ) Host-Gut Microbiota Metabolic Interactions. Science 336: 1262–1267 doi:10.1126/science.1223813

    Not in our library10.1126/science.1223813

  2. 2.

    Krause DO, Denman SE, Mackie RI, Morrison M, Rae AL, et al (2003 ) Opportunities to improve fiber degradation in the rumen: microbiology, ecology, and genomics. FEMS Microbiology Reviews 27: 663–693 doi:10.1016/S0168-6445(03)00072-X

    Not in our library10.1016/s0168-6445(03)00072-x

  3. 3.

    McFall-Ngai M, Heath-Heckman EAC, Gillette AA, Peyer SM, Harvie EA (2012 ) The secret languages of coevolved symbioses: Insights from the Euprymna scolopes–Vibrio fischeri symbiosis. Seminars in Immunology 24: 3–8 doi:10.1016/j.smim.2011.11.006

    Not in our library10.1016/j.smim.2011.11.006

  4. 4.

    Oliver KM, Russell JA, Moran NA, Hunter MS (2003 ) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences 100: 1803–1807.

    Not in our library10.1073/pnas.0335320100

  5. 5.

    Kaltenpoth M, Göttler W, Herzner G, Strohm E (2005 ) Symbiotic bacteria protect wasp larvae from fungal infestation. Current Biology 15: 475–479.

    Not in our library10.1016/j.cub.2004.12.084

  6. 6.

    Kaiser W, Huguet E, Casas J, Commin C, Giron D (2010 ) Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proceedings of the Royal Society B: Biological Sciences 277: 2311–2319 doi:10.1098/rspb.2010.0214

    Not in our library10.1098/rspb.2010.0214

  7. 7.

    Galac MR, Lazzaro BP (2011 ) Comparative pathology of bacteria in the genus Providencia to a natural host, Drosophila melanogaster. Microbes and Infection 13: 673–683 doi:10.1016/j.micinf.2011.02.005

    Not in our library10.1016/j.micinf.2011.02.005

  8. 8.

    Hurst GDD, Johnson AP, Schulenburg JHG, Fuyama Y (2000 ) Male-Killing Wolbachia in Drosophila: A Temperature-Sensitive Trait With a Threshold Bacterial Density. Genetics 156: 699–709.

    Not in our library10.1093/genetics/156.2.699

  9. 9.

    Ferrari J, Vavre F (2011 ) Bacterial symbionts in insects or the story of communities affecting communities. Philosophical Transactions of the Royal Society B: Biological Sciences 366: 1389–1400 doi:10.1098/rstb.2010.0226

    Not in our library10.1098/rstb.2010.0226

  10. 10.

    Staubach F, Künzel S, Baines AC, Yee A, McGee BM, et al (2012 ) Expression of the blood-group-related glycosyltransferase B4galnt2 influences the intestinal microbiota in mice. The ISME Journal 6: 1345–1355.

    Not in our library10.1038/ismej.2011.204

  11. 11.

    Bakula M (1969 ) The persistence of a microbial flora during postembryogenesis of Drosophila melanogaster. Journal of invertebrate pathology 14: 365–374.

    Not in our library10.1016/0022-2011(69)90163-3

  12. 12.

    Ryu JH, Kim SH, Lee HY, Bai JY, Nam YD, et al (2008 ) Innate Immune Homeostasis by the Homeobox Gene Caudal and Commensal-Gut Mutualism in Drosophila. Science 319: 777–782 doi:10.1126/science.1149357

    Not in our library10.1126/science.1149357

  13. 13.

    Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, et al (2011 ) Enterotypes of the human gut microbiome. Nature 473: 174–180.

    Not in our library10.1038/nature09944

  14. 14.

    Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y-Y, et al (2011 ) Linking Long-Term Dietary Patterns with Gut Microbial Enterotypes. Science 334: 105–108 doi:10.1126/science.1208344

    Not in our library10.1126/science.1208344

  15. 15.

    Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, et al (2008 ) Evolution of Mammals and Their Gut Microbes. Science 320: 1647–1651 doi:10.1126/science.1155725

    Not in our library10.1126/science.1155725

  16. 16.
  17. 17.

    Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, et al (2011 ) Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans. Science 332: 970–974 doi:10.1126/science.1198719

    Not in our library10.1126/science.1198719

  18. 18.

    Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, et al (2012 ) Human gut microbiome viewed across age and geography. Nature 486: 222–228 doi:10.1038/nature11053

    Not in our library10.1038/nature11053

  19. 19.

    Fraune S, Abe Y, Bosch TCG (2009 ) Disturbing epithelial homeostasis in the metazoan Hydra leads to drastic changes in associated microbiota. Environmental Microbiology 11: 2361–2369 doi:10.1111/j.1462-2920.2009.01963.x

    Not in our library10.1111/j.1462-2920.2009.01963.x

  20. 20.

    Wong CNA, Ng P, Douglas AE (2011 ) Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environmental Microbiology 13: 1889–1900 doi:10.1111/j.1462-2920.2011.02511.x

    Not in our library10.1111/j.1462-2920.2011.02511.x

  21. 21.

    Broderick N, Lemaitre B (2012 ) Gut-associated microbes of Drosophila melanogaster. Gut microbes 3: 307–321.

    Not in our library10.4161/gmic.19896

  22. 22.

    Erkosar B, Storelli G, Defaye A, Leulier F (2013 ) Host-intestinal microbiota mutualism:“learning on the fly”. Cell host & microbe 13: 8–14.

    Not in our library10.1016/j.chom.2012.12.004

  23. 23.

    Lemaitre B, Hoffmann J (2007 ) The Host Defense of Drosophila melanogaster. Annual Review of Immunology 25: 697–743 doi:10.1146/annurev.immunol.25.022106.141615

    Not in our library10.1146/annurev.immunol.25.022106.141615

  24. 24.

    Stensmyr MC, Dweck HKM, Farhan A, Ibba I, Strutz A, et al (2012 ) A Conserved Dedicated Olfactory Circuit for Detecting Harmful Microbes in Drosophila. Cell 151: 1345–1357 doi:10.1016/j.cell.2012.09.046

    Not in our library10.1016/j.cell.2012.09.046

  25. 25.

    Lazzaro BP, Sceurman BK, Clark AG (2004 ) Genetic Basis of Natural Variation in D. melanogaster Antibacterial Immunity. Science 303: 1873–1876 doi:10.1126/science.1092447

    Not in our library10.1126/science.1092447

  26. 26.

    Lhocine N, Ribeiro PS, Buchon N, Wepf A, Wilson R, et al (2008 ) PIMS Modulates Immune Tolerance by Negatively Regulating Drosophila Innate Immune Signaling. Cell Host & Microbe 4: 147–158 doi:10.1016/j.chom.2008.07.004

    Not in our library10.1016/j.chom.2008.07.004

  27. 27.

    Shin SC, Kim SH, You H, Kim B, Kim AC, et al (2011 ) Drosophila Microbiome Modulates Host Developmental and Metabolic Homeostasis via Insulin Signaling. Science 334: 670–674 doi:10.1126/science.1212782

    Not in our library10.1126/science.1212782

  28. 28.

    Storelli G, Defaye A, Erkosar B, Hols P, Royet J, et al (2011 ) Lactobacillus plantarum Promotes Drosophila Systemic Growth by Modulating Hormonal Signals through TOR-Dependent Nutrient Sensing. Cell Metabolism 14: 403–414 doi:10.1016/j.cmet.2011.07.012

    Not in our library10.1016/j.cmet.2011.07.012

  29. 29.

    Ren C, Webster P, Finkel SE, Tower J (2007 ) Increased Internal and External Bacterial Load during Drosophila Aging without Life-Span Trade-Off. Cell Metabolism 6: 144–152 doi:10.1016/j.cmet.2007.06.006

    Not in our library10.1016/j.cmet.2007.06.006

  30. 30.

    Cox CR, Gilmore MS (2007 ) Native Microbial Colonization of Drosophila melanogaster and Its Use as a Model of Enterococcus faecalis Pathogenesis. Infection and Immunity 75: 1565–1576 doi:10.1128/IAI.01496-06

    Not in our library10.1128/iai.01496-06

  31. 31.

    Corby-Harris V, Pontaroli AC, Shimkets LJ, Bennetzen JL, Habel KE, et al (2007 ) Geographical Distribution and Diversity of Bacteria Associated with Natural Populations of Drosophila melanogaster. Applied and Environmental Microbiology 73: 3470–3479 doi:10.1128/AEM.02120-06

    Not in our library10.1128/aem.02120-06

  32. 32.
  33. 33.

    Barata A, Santos SC, Malfeito-Ferreira M, Loureiro V (2012 ) New Insights into the Ecological Interaction Between Grape Berry Microorganisms and Drosophila Flies During the Development of Sour Rot. Microbial Ecology 64: 416–430 doi:10.1007/s00248-012-0041-y

    Not in our library10.1007/s00248-012-0041-y

  34. 34.

    Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, et al (2007 ) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203–218 doi:10.1038/nature06341

    Not in our library10.1038/nature06341

  35. 35.

    Simpson EH (1949 ) Measurement of Diversity. Nature 163: 688–688.

    Not in our library

  36. 36.

    Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, et al (2007 ) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Research 35: 7188–7196 doi:10.1093/nar/gkm864

    Not in our library10.1093/nar/gkm864

  37. 37.

    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al (2009 ) Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Applied and Environmental Microbiology 75: 7537–7541 doi:10.1128/AEM.01541-09

    Not in our library10.1128/aem.01541-09

  38. 38.

    Juneja P, Lazzaro BP (2009 ) Providencia sneebia sp. nov. and Providencia burhodogranariea sp. nov., isolated from wild Drosophila melanogaster. International Journal of Systematic and Evolutionary Microbiology 59: 1108–1111 doi:10.1099/ijs.0.000117-0

    Not in our library10.1099/ijs.0.000117-0

  39. 39.

    Ravussin Y, Koren O, Spor A, LeDuc C, Gutman R, et al (2011 ) Responses of Gut Microbiota to Diet Composition and Weight Loss in Lean and Obese Mice. Obesity 20: 738–747 doi:10.1038/oby.2011.111

    Not in our library10.1038/oby.2011.111

  40. 40.

    Dabbah R, Edwards VM, Moats WA (1970 ) Antimicrobial action of some citrus fruit oils on selected food-borne bacteria. Applied microbiology 19: 27–31.

    Not in our library10.1128/am.19.1.27-31.1970

  41. 41.

    Nunney L (1996 ) The colonization of oranges by the cosmopolitan Drosophila. Oecologia 108: 552–561.

    Not in our library10.1007/bf00333733

  42. 42.

    Young TP, Chase JM, Huddleston RT (2001 ) Community succession and assembly comparing, contrasting and combining paradigms in the context of ecological restoration. Ecological Restoration 19: 5–18.

    Not in our library

  43. 43.

    Lazzaro BP, Sackton TB, Clark AG (2006 ) Genetic Variation in Drosophila melanogaster Resistance to Infection: A Comparison Across Bacteria. Genetics 174: 1539–1554 doi:10.1534/genetics.105.054593

    Not in our library10.1534/genetics.105.054593

  44. 44.

    Deppenmeier U, Hoffmeister M, Prust C (2002 ) Biochemistry and biotechnological applications of Gluconobacter strains. Applied Microbiology and Biotechnology 60: 233–242 doi:10.1007/s00253-002-1114-5

    Not in our library10.1007/s00253-002-1114-5

  45. 45.

    Crotti E, Rizzi A, Chouaia B, Ricci I, Favia G, et al (2010 ) Acetic Acid Bacteria, Newly Emerging Symbionts of Insects. Applied and Environmental Microbiology 76: 6963–6970 doi:10.1128/AEM.01336-10

    Not in our library10.1128/aem.01336-10

  46. 46.

    De Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, et al.. (2009) Bergey's Manual of Systematic Bacteriology: Volume 3: The Firmicutes. Springer.

    Not in our library

  47. 47.

    Rao RS, Bhadra B, Shivaji S (2008 ) Isolation and characterization of ethanol-producing yeasts from fruits and tree barks. Letters in Applied Microbiology 47: 19–24 doi:10.1111/j.1472-765X.2008.02380.x

    Not in our library10.1111/j.1472-765x.2008.02380.x

  48. 48.

    Vellend M (2010 ) Conceptual Synthesis in Community Ecology. The Quarterly Review of Biology 85: 183–206.

    Not in our library10.1086/652373

  49. 49.

    Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, et al (2010 ) Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of the National Academy of Sciences 107: 20051–20056 doi:10.1073/pnas.1009906107

    Not in our library10.1073/pnas.1009906107

  50. 50.

    Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press.

    Not in our library10.1016/j.tree.2011.03.024

  51. 51.

    Peay KG, Belisle M, Fukami T (2011 ) Phylogenetic relatedness predicts priority effects in nectar yeast communities. Proceedings of the Royal Society B: Biological Sciences 279: 749–758 doi:10.1098/rspb.2011.1230

    Not in our library10.1098/rspb.2011.1230

  52. 52.

    Linderman JA, Chambers MC, Gupta AS, Schneider DS (2012 ) Infection-Related Declines in Chill Coma Recovery and Negative Geotaxis in Drosophila melanogaster. PLoS ONE 7: e41907 doi:10.1371/journal.pone.0041907

    Not in our library10.1371/journal.pone.0041907

  53. 53.

    Tsiropoulos GJ (1983 ) Microflora associated with wild and laboratory reared adult olive fruit flies, Dacus oleae (Gmel.). Zeitschrift für Angewandte Entomologie 96: 337–340.

    Not in our library

  54. 54.

    Kunin V, Engelbrektson A, Ochman H, Hugenholtz P (2010 ) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environmental Microbiology 12: 118–123 doi:10.1111/j.1462-2920.2009.02051.x

    Not in our library10.1111/j.1462-2920.2009.02051.x

  55. 55.

    Auld RR, Myre M, Mykytczuk NCS, Leduc LG, Merritt TJS (2013 ) Characterization of the microbial acid mine drainage microbial community using culturing and direct sequencing techniques. Journal of Microbiological Methods 93: 108–115 doi:10.1016/j.mimet.2013.01.023

    Not in our library10.1016/j.mimet.2013.01.023

  56. 56.

    Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007 ) The role of microorganisms in coral health, disease and evolution. Nature Reviews Microbiology 5: 355–362 doi:10.1038/nrmicro1635

    Not in our library10.1038/nrmicro1635

  57. 57.

    O'Hara AM, Shanahan F (2006 ) The gut flora as a forgotten organ. EMBO reports 7: 688–693 doi:10.1038/sj.embor.7400731

    Not in our library10.1038/sj.embor.7400731

  58. 58.

    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011 ) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194–2200 doi:10.1093/bioinformatics/btr381

    Not in our library10.1093/bioinformatics/btr381

  59. 59.

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