Bacterial Communities of Diverse Species: Ecological Context of a Host–Microbe Model System

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Drosophila melanogaster is emerging as an important model of non-pathogenic host–microbe interactions. The genetic and experimental tractability of Drosophila has led to significant gains in our understanding of animal–microbial symbiosis. However, the full implications of these results cannot be appreciated without the knowledge of the microbial communities associated with natural Drosophila populations. In particular, it is not clear whether laboratory cultures can serve as an accurate model of host–microbe interactions that occur in the wild, or those that have occurred over evolutionary time. To fill this gap, we characterized natural bacterial communities associated with 14 species of Drosophila and related genera collected from distant geographic locations. To represent the ecological diversity of Drosophilids, examined species included fruit-, flower-, mushroom-, and cactus-feeders. In parallel, wild host populations were compared to laboratory strains, and controlled experiments were performed to assess the importance of host species and diet in shaping bacterial microbiome composition. We find that Drosophilid flies have taxonomically restricted bacterial communities, with 85% of the natural bacterial microbiome composed of only four bacterial families. The dominant bacterial taxa are widespread and found in many different host species despite the taxonomic, ecological, and geographic diversity of their hosts. Both natural surveys and laboratory experiments indicate that host diet plays a major role in shaping the Drosophila bacterial microbiome. Despite this, the internal bacterial microbiome represents only a highly reduced subset of the external bacterial communities, suggesting that the host exercises some level of control over the bacteria that inhabit its digestive tract. Finally, we show that laboratory strains provide only a limited model of natural host–microbe interactions. Bacterial taxa used in experimental studies are rare or absent in wild Drosophila populations, while the most abundant associates of natural Drosophila populations are rare in the lab.

Vyšlo v časopise: Bacterial Communities of Diverse Species: Ecological Context of a Host–Microbe Model System. PLoS Genet 7(9): e32767. doi:10.1371/journal.pgen.1002272
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002272

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1. MarkowTAO'GradyP 2006 Drosophila: A guide to species identification and use. Oxford, UK Elsevier

2. JonesCD 2005 The genetics of adaptation in Drosophila sechellia. Genetica 123 137 145

3. MarkowTAO'GradyP 2008 Reproductive ecology of Drosophila. Functional Ecology 22 747 759

4. MarkowTAO'GradyPM 2005 Evolutionary genetics of reproductive behavior in Drosophila: Connecting the dots. Annual Review of Genetics 39 263 291

5. JaenikeJ 1985 Parasite Pressure and the Evolution of Amanitin Tolerance in Drosophila. Evolution 39 1295 1301

6. SpicerGSJaenikeJ 1996 Phylogenetic analysis of breeding site use and alpha-amanitin tolerance within the Drosophila quinaria species group. Evolution 50 2328 2337

7. MagnaccaKNFooteDO'GradyPM 2008 A review of the endemic Hawaiian Drosophilidae and their host plants. Zootaxa 1 58

8. WuDDaughertySCVan AkenSEPaiGHWatkinsKL 2006 Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol 4 e188 doi:10.1371/journal.pbio.0040188.

9. MoranNA 2002 The ubiquitous and varied role of infection in the lives of animals and plants. American Naturalist 160 S1 S8

10. TurnbaughPJLeyREHamadyMFraser-LiggettCMKnightR 2007 The human microbiome project. Nature 449 804 810

11. LeyRETurnbaughPJKleinSGordonJI 2006 Human gut microbes associated with obesity. Nature 444 1022 1023

12. LeyREHamadyMLozuponeCTurnbaughPJRameyRR 2008 Evolution of mammals and their gut microbes. Science 320 1647 1651

13. BrooksMA 1963 The microorganisms of healthy insects. SteinhausEA Insect Pathology: An Advanced Treatise London Academic Press

14. DillonRJDillonVM 2004 The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49 71 92

15. JansonEMStiremanJO3rdSingerMSAbbotP 2008 Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification. Evolution 62 997 1012

16. BruneA 1998 Termite guts: the world's smallest bioreactors. Trends Biotechnol 16 16 21

17. HosokawaTKikuchiYNikohNShimadaMFukatsuT 2006 Strict Host-Symbiont Cospeciation and Reductive Genome Evolution in Insect Gut Bacteria. PLoS Biol 4 e337 doi:10.1371/journal.pbio.0040337

18. KaufmanMGKlugMJ 1991 The Contribution of Hindgut Bacteria to Dietary Carbohydrate Utilization by Crickets (Orthoptera, Gryllidae). Comparative Biochemistry and Physiology a-Physiology 98 117 123

19. BroderickNARaffaKFHandelsmanJ 2006 Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proceedings of the National Academy of Sciences of the United States of America 103 15196 15199

20. LeyREBackhedFTurnbaughPLozuponeCAKnightRD 2005 Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences of the United States of America 102 11070 11075

21. RyuJHKimSHLeeHYBaiJYNamYD 2008 Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila. Science 319 777 782

22. RawlsJFMahowaldMALeyREGordonJI 2006 Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127 423 433

23. HosokawaTKikuchiYShimadaMFukatsuT 2007 Obligate symbiont involved in pest status of host insect. Proceedings of the Royal Society B-Biological Sciences 274 1979 1984

24. NodaSKitadeOInoueTKawaiMKanukaM 2007 Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), their hosts, and their bacterial endosymbionts. Molecular Ecology 16 1257 1266

25. De FilippoCCavalieriDDi PaolaMRamazzottiMPoulletJB 2010 Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proceedings of the National Academy of Sciences of the United States of America 107 14691 14696

26. LhocineNRibeiroPSBuchonNWepfAWilsonR 2008 PIMS modulates immune tolerance by negatively regulating Drosophila innate immune signaling. Cell Host & Microbe 4 147 158

27. BrummelTChingASeroudeLSimonAFBenzerS 2004 Drosophila lifespan enhancement by exogenous bacteria. Proceedings of the National Academy of Sciences of the United States of America 101 12974 12979

28. RenCWebsterPFinkelSETowerJ 2007 Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metabolism 6 144 152

29. SharonGSegalDRingoJMHefetzAZilber-RosenbergI 2010 Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America 107 20051 20056

30. BroderickNARaffaKFGoodmanRMHandelsmanJ 2004 Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol 70 293 300

31. XiangHWeiGFJiaSHuangJMiaoXX 2006 Microbial communities in the larval midgut of laboratory and field populations of cotton bollworm (Helicoverpa armigera). Can J Microbiol 52 1085 1092

32. CoxCRGilmoreMS 2007 Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infection and Immunity 75 1565 1576

33. Corby-HarrisVPontaroliACShimketsLJBennetzenJLHabelKE 2007 Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster. Applied and Environmental Microbiology 73 3470 3479

34. HillJESeippRPBettsMHawkinsLVan KesselAG 2002 Extensive profiling of a complex microbial community by high-throughput sequencing. Applied and Environmental Microbiology 68 3055 3066

35. SchlossPDWestcottSLRyabinTHallJRHartmannM 2009 Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Applied and Environmental Microbiology 75 7537 7541

36. PriceMNDehalPSArkinAP 2010 FastTree 2-Approximately Maximum-Likelihood Trees for Large Alignments. PLoS ONE 5 e9490 doi:10.1371/journal.pone.0009490

37. JunejaPLazzaroBP 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

38. DouglasAE 1998 Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology 43 17 37

39. OliverKMRussellJAMoranNAHunterMS 2003 Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences of the United States of America 100 1803 1807

40. MontllorCBMaxmenAPurcellAH 2002 Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecological Entomology 27 189 195

41. MoranNARussellJAKogaRFukatsuT 2005 Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Applied and Environmental Microbiology 71 3302 3310

42. VolkmannMSkiebeEKerrinnesTFaberFLepkaD 2010 Orbus hercynius gen. nov., sp. nov., isolated from faeces of wild boar, is most closely related to members of the orders ‘Enterobacteriales’ and Pasteurellales. International Journal of Systematic and Evolutionary Microbiology 60 2601 2605

43. JeyaprakashAHoyMAAllsoppMH 2003 Bacterial diversity in worker adults of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) assessed using 16S rRNA sequences. Journal of Invertebrate Pathology 84 96 103

44. BabendreierDJollerDRomeisJBiglerFWidmerF 2007 Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. Fems Microbiology Ecology 59 600 610

45. YoshiyamaMKimuraK 2009 Bacteria in the gut of Japanese honeybee, Apis cerana japonica, and their antagonistic effect against Paenibacillus larvae, the causal agent of American foulbrood. Journal of Invertebrate Pathology 102 91 96

46. OlofssonTCVasquezA 2008 Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Current Microbiology 57 356 363

47. JandaJMAbbottSL 2006 The Enterobacteria. 2nd ed. Washington, DC ASM Press

48. LazzaroBPSacktonTBClarkAG 2006 Genetic variation in Drosophila melanogaster resistance to infection: A comparison across bacteria. Genetics 174 1539 1554

49. KerstersKLisdiyantaPKomagataKSwingsJ 2006 The Familly Acetobacteraceae: The Genera Acetobacter, Acidomonas, Asaia, Gluconacetobacter, Gluconobacter, and Kozakia. FalkowSRosenbergESchleiferK-HStackebrandtEDworkinM The Prokaryotes New York, NY Springer Science+Business Media, LLC 163 200

50. CrottiERizziAChouaiaBRicciIFaviaG 2010 Acetic Acid Bacteria, Newly Emerging Symbionts of Insects. Applied and Environmental Microbiology 76 6963 6970

51. LjunghAWadstromT 2009 Lactobacillus Molecular Biology: From Genomics to Probiotics. Norfolk, UK Caister Academic Press

52. HammesWPHertelC 2006 The Genera Lactobacillus and Carnobacterium. FalkowSRosenbergESchleiferK-HStackebrandtEDworkinM The Prokaryotes New York, NY Springer Science+Business Media, LLC 320 403

53. GilmoreMS 2002 The Enterococci: pathogenesis, molecular biology, and antibiotic resistance. Washington, DC ASM Press

54. EgertMWagnerBLemkeTBruneAFriedrichMW 2003 Microbial community structure in midgut and hindgut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Applied and Environmental Microbiology 69 6659 6668

55. AkmanLYamashitaAWatanabeHOshimaKShibaT 2002 Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nature Genetics 32 402 407

56. KlassonLWestbergJSapountzisPNasiundKLutnaesY 2009 The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proceedings of the National Academy of Sciences of the United States of America 106 5725 5730

57. KageyamaDAnbutsuHWatadaMHosokawaTShimadaM 2006 Prevalence of a non-male-killing spiroplasma in natural populations of Drosophila hydei. Applied and Environmental Microbiology 72 6667 6673

58. HaselkornTSMarkowTAMoranNA 2009 Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Molecular Ecology 18 1294 1305

59. ChaoA 1984 Non-parametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11 6

60. BikEMLongCDArmitageGCLoomerPEmersonJ 2010 Bacterial diversity in the oral cavity of 10 healthy individuals. Isme Journal 4 962 974

61. LozuponeCHamadyMKnightR 2006 UniFrac - An online tool for comparing microbial community diversity in a phylogenetic context. Bmc Bioinformatics 7 -

62. HamadyMLozuponeCKnightR 2010 Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. Isme Journal 4 17 27

63. KounatidisICrottiESapountzisPSacchiLRizziA 2009 Acetobacter tropicalis Is a Major Symbiont of the Olive Fruit Fly (Bactrocera oleae). Applied and Environmental Microbiology 75 3281 3288

64. AshboltNJInkermanPA 1990 Acetic-Acid Bacterial Biota of the Pink Sugar-Cane Mealybug, Saccharococcus-Sacchari, and Its Environs. Applied and Environmental Microbiology 56 707 712

65. MohrKITebbeCC 2006 Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environmental Microbiology 8 258 272

66. ZouacheKVoroninDTran-VanVMavinguiP 2009 Composition of Bacterial Communities Associated with Natural and Laboratory Populations of Asobara tabida Infected with Wolbachia. Applied and Environmental Microbiology 75 3755 3764

67. SchlossPDDelaliberaIHandelsmanJRaffaKF 2006 Bacteria associated with the guts of two wood-boring beetles: Anoplophora glabripennis and Saperda vestita (Cerambycidae). Environmental Entomology 35 625 629

68. VasanthakumarADelaliberaIHandelsmanJKlepzigKDSchlossPD 2006 Characterization of gut-associated bacteria in larvae and adults of the southern pine beetle, Dendroctonus frontalis Zimmermann. Environmental Entomology 35 1710 1717

69. LehmanRLundgrenJPetzkeL 2009 Bacterial Communities Associated with the Digestive Tract of the Predatory Ground Beetle, Poecilus chalcites, and Their Modification by Laboratory Rearing and Antibiotic Treatment. Microbial Ecology 57 349 358

70. RussellJAMoreauCSGoldman-HuertasBFujiwaraMLohmanDJ 2009 Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proceedings of the National Academy of Sciences of the United States of America 106 21236 21241

71. BurkeGRNormarkBBFavretCMoranNA 2009 Evolution and Diversity of Facultative Symbionts from the Aphid Subfamily Lachninae. Applied and Environmental Microbiology 75 5328 5335

72. LatorreALamelasAPerez-BrocalVGomez-ValeroLGosalbesMJ 2008 Evolution of the secondary symbiont “Candidatus Serratia symbiotica” in aphid species of the subfamily Lachninae. Applied and Environmental Microbiology 74 4236 4240

73. LeyRELozuponeCAHamadyMKnightRGordonJI 2008 Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Reviews Microbiology 6 776 788

74. OchmanHWorobeyMKuoCHNdjangoJBNPeetersM 2010 Evolutionary Relationships of Wild Hominids Recapitulated by Gut Microbial Communities. PLoS Biol 8 e1000546 doi:10.1371/journal.pbio.1000546

75. GuichardAParkJMCruz-MorenoBKarinMBierE 2006 Anthrax lethal factor and edema factor act on conserved targets in Drosophila. Proc Natl Acad Sci U S A 103 3244 3249

76. BlowNSSalomonRNGarrityKReveillaudIKopinA 2005 Vibrio cholerae infection of Drosophila melanogaster mimics the human disease cholera. PLoS Pathog 1 e8 doi:10.1371/journal.ppat.0010008

77. ParkSYHeoYJKimKSChoYH 2005 Drosophila melanogaster is susceptible to Vibrio cholerae infection. Mol Cells 20 409 415

78. SchneiderDSAyresJSBrandtSMCostaADionneMS 2007 Drosophila eiger mutants are sensitive to extracellular pathogens. PLoS Pathog 3 e41 doi:10.1371/journal.ppat.0030041

79. PhamLNDionneMSShirasu-HizaMSchneiderDS 2007 A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 3 e26 doi:10.1371/journal.ppat.0030026

80. BrandtSMDionneMSKhushRSPhamLNVigdalTJ 2004 Secreted bacterial effectors and host-produced eiger/TNF drive death in a Salmonella-infected fruit fly. PLoS Biol 2 e418 doi:10.1371/journal.pbio.0020418

81. FauvarqueMOBergeretEChabertJDacheuxDSatreM 2002 Role and activation of type III secretion system genes in Pseudomonas aeruginosa-induced Drosophila killing. Microb Pathog 32 287 295

82. LauGWGoumnerovBCWalendziewiczCLHewitsonJXiaoW 2003 The Drosophila melanogaster toll pathway participates in resistance to infection by the gram-negative human pathogen Pseudomonas aeruginosa. Infect Immun 71 4059 4066

83. EricksonDLLinesJLPesciECVenturiVStoreyDG 2004 Pseudomonas aeruginosa relA contributes to virulence in Drosophila melanogaster. Infect Immun 72 5638 5645

84. ApidianakisYMindrinosMNXiaoWLauGWBaldiniRL 2005 Profiling early infection responses: Pseudomonas aeruginosa eludes host defenses by suppressing antimicrobial peptide gene expression. Proc Natl Acad Sci U S A 102 2573 2578

85. Avet-RochexABergeretEAttreeIMeisterMFauvarqueMO 2005 Suppression of Drosophila cellular immunity by directed expression of the ExoS toxin GAP domain of Pseudomonas aeruginosa. Cell Microbiol 7 799 810

86. KocksCChoJHNehmeNUlvilaJPearsonAM 2005 Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 123 335 346

87. FlygCKenneKBomanHG 1980 Insect pathogenic properties of Serratia marcescens: phage-resistant mutants with a decreased resistance to Cecropia immunity and a decreased virulence to Drosophila. J Gen Microbiol 120 173 181

88. BassetATzouPLemaitreBBoccardF 2003 A single gene that promotes interaction of a phytopathogenic bacterium with its insect vector, Drosophila melanogaster. EMBO Rep 4 205 209

89. BassetAKhushRSBraunAGardanLBoccardF 2000 The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc Natl Acad Sci U S A 97 3376 3381

90. DionneMSSchneiderDS 2008 Models of infectious diseases in the fruit fly Drosophila melanogaster. Dis Model Mech 1 43 49

91. VodovarNVinalsMLiehlPBassetADegrouardJ 2005 Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc Natl Acad Sci U S A 102 11414 11419

92. LiehlPBlightMVodovarNBoccardFLemaitreB 2006 Prevalence of local immune response against oral infection in a Drosophila/Pseudomonas infection model. PLoS Pathog 2 e56 doi:10.1371/journal.ppat.0020056

93. McOristALJacksonMBirdAR 2002 A comparison of five methods for extraction of bacterial DNA from human faecal samples. Journal of Microbiological Methods 50 131 139

94. BakerGCSmithJJCowanDA 2003 Review and re-analysis of domain-specific 16S primers. Journal of Microbiological Methods 55 541 555

95. SchlossPD 2010 The Effects of Alignment Quality, Distance Calculation Method, Sequence Filtering, and Region on the Analysis of 16S rRNA Gene-Based Studies. PLoS Comput Biol 6 e1000844 doi:10.1371/journal.pcbi.1000844

96. EwingBHillierLWendlMCGreenP 1998 Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Research 8 175 185

97. EwingBGreenP 1998 Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Research 8 186 194

98. NawrockiEPKolbeDLEddySR 2009 Infernal 1.0: inference of RNA alignments. Bioinformatics 25 1335 1337

99. SchlossPDHandelsmanJ 2005 Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied and Environmental Microbiology 71 1501 1506

100. ColeJRWangQCardenasEFishJChaiB 2009 The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Research 37 D141 D145

101. SoltisDESoltisPS 2003 The role of phylogenetics in comparative genetics. Plant Physiology 132 1790 1800

102. HusonDHRichterDCRauschCDezulianTFranzM 2007 Dendroscope: An interactive viewer for large phylogenetic trees. Bmc Bioinformatics 8 -

103. KuczynskiJCostelloEKNemergutDRZaneveldJLauberCL 2010 Direct sequencing of the human microbiome readily reveals community differences. Genome Biology 11 -

104. ChaffronSRehrauerHPernthalerJvon MeringC 2010 A global network of coexisting microbes from environmental and whole-genome sequence data. Genome Research 20 947 959