Abstract
Animals are routinely colonized by microorganisms. Despite many studies documenting the microbial taxa associated with animals, the pattern and ecological determinants of among-animal variation in microbial communities are poorly understood. This study quantified the bacterial communities associated with natural populations of Drosophila melanogaster. Across five collections, each fly bore 16–78 OTUs, predominantly of the Acetobacteraceae, Lactobacillaceae, and Enterobacteriaceae. Positive relationships, mostly among related OTUs, dominated both the significant co-occurrences and co-association networks among bacteria, and OTUs with important network positions were generally of intermediate abundance and prevalence. The prevalence of most OTUs was well predicted by a neutral model suggesting that ecological drift and passive dispersal contribute significantly to microbiome composition. However, some Acetobacteraceae and Lactobacillaceae were present in more flies than predicted, indicative of superior among-fly dispersal. These taxa may be well-adapted to the Drosophila habitat from the perspective of dispersal as the principal benefit of the association to the microbial partners. Taken together, these patterns indicate that both stochastic processes and deterministic processes relating to the differential capacity for persistence in the host habitat and transmission between hosts contribute to bacterial community assembly in Drosophila melanogaster.
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References
Vellend M. Conceptual synthesis in community ecology. Q Rev Biol. 2010;85:183–206.
Degnan PH, Pusey AE, Lonsdorf EV, Goodall J, Wroblewski EE, Wilson ML, et al. Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proc Natl Acad Sci USA. 2012;109:13034–9.
Osei-Poku J, Mbogo CM, Palmer WJ, Jiggins FM. Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from Kenya. Mol Ecol. 2012;21:5138–50.
Smith CCR, Snowberg LK, Caporaso GJ, Knight R, Bolnick DI. Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota. ISME J. 2015;9:1–12.
Steelman SM, Chowdhary BP, Dowd S, Suchodolski J, Janečka JE. Pyrosequencing of 16S rRNA genes in fecal samples reveals high diversity of hindgut microflora in horses and potential links to chronic laminitis. BMC Vet Res. 2012;8:231.
Jeraldo P, Sipos M, Chia N, Brulc JM, Dhillon AS, Konkel ME, et al. Quantification of the relative roles of niche and neutral processes in structuring gastrointestinal microbiomes. Proc Natl Acad Sci USA. 2012;109:9692–8.
Li L, Ma Z. Testing the neutral theory of biodiversity with human microbiome datasets. Sci Rep. 2016;6:31448.
Burns AR, Stephens WZ, Stagaman K, Wong S, Rawls JF, Guillemin K, et al. Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J. 2016;10:655–64.
Venkataraman A, Bassis CM, Beck JM, Young VB, Curtis JL, Huffnagle GB, et al. Application of a neutral community model to assess structuring of the human lung microbiome. mBio. 2015;6:e02284–14.
Newell PD, Douglas AE. Interspecies interactions determine the impact of the gut microbiota on nutrient allocation in Drosophila melanogaster. Appl Environ Microbiol. 2014;80:788–96.
Wong AC-N, Chaston JM, Douglas AE. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J. 2013;7:1922–32.
Chaston JM, Dobson AJ, Newell PD, Douglas AE. Host genetic control of the microbiota mediates the Drosophila nutritional phenotype. Appl Environ Microbiol. 2016;82:671–9.
Broderick NA, Buchon N, Lemaitre B. Microbiota-induced changes in Drosophila melanogaster host gene expression and gut morphology. mBio. 2014;5:e01117–14.
Obadia B, Guvener ZY, Zhang V, Ceja-Navarro JA, Brodie EL, Ja WW, Ludington WB. Probabilistic invasion underlies natural gut microbiome stability. Curr Biol. 2017;27:1999–2006.e8.
Chandler JA, Morgan Lang J, Bhatnagar S, Eisen JA, Kopp A. Bacterial communities of diverse Drosophila species: ecological context of a host–microbe model system. PLoS Genet. 2011;7:e1002272.
Staubach F, Baines JF, Künzel S, Bik EM, Petrov DA. Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment. PLoS ONE. 2013;8:e70749.
Martinson VG, Douglas AE, Jaenike J. Community structure of the gut microbiota in sympatric species of wild Drosophila. Ecol Lett. 2017;20:629–39.
Ren C, Webster P, Finkel SE, Tower J. Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metab. 2007;6:144–52.
Pietri JE, DeBruhl H, Sullivan W. The rich somatic life of Wolbachia. Microbiol Open. 2016;5:923–36.
Layeghifard M, Hwang DM, Guttman DS. Disentangling interactions in the microbiome: a network perspective. Trends Microbiol. 2017;25:217–28.
Cardona C, Weisenhorn P, Henry C, Gilbert JA. Network-based metabolic analysis and microbial community modeling. Curr Opin Microbiol. 2016;31:124–31.
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112–20.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.
Aronesty E. Comparison of sequencing utility programs. Open Bioinf J. 2013;7:1–8.
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.
Rideout JR, He Y, Navas-Molina JA, Walters WA, Ursell LK, Gibbons SM, et al. Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. PeerJ. 2014;2:e545.
R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2015.
Hsieh TC, Ma KH, Chao A. iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0.8; 2016.
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. nlme: linear and nonlinear mixed effects models. R package version 3; 2016: 1–128.
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM. Mixed effects models and extensions in ecology with R. New York, NY; 2009.
Legendre P, Anderson M. Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr. 1999;69:1–24.
McArdle B, Anderson M. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology. 2001;82:290–7.
Legendre P, Oksanen J, ter Braak CJF. Testing the significance of canonical axes in redundancy analysis. Methods Ecol Evol. 2011;2:269–77.
Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P, Minchin PR, O’Hara RB et al. Vegan: community ecology package. R package version 2. 2016: 3–4.
Veech JA. A probabilistic model for analysing species co-occurrence. Glob Ecol Biogeogr. 2013;22:252–60.
Griffith DM, Veech JA, Marsh CJ. cooccur: probabilistic species co-occurrence analysis in R. J Stat Softw. 2016;69:1–17.
Kurtz ZD, Müller CL, Miraldi ER, Littman DR, Blaser MJ, Bonneau RA. Sparse and compositionally robust inference of microbial ecological networks. PLoS Comput Biol. 2015;11:1–25.
Meinshausen N, Bühlmann P. High-dimensional graphs and variable selection with the Lasso. Ann Stat. 2006;34:1436–62.
Csardi G, Nepusz T. The igraph software package for complex network research. Inter J Complex Syst: 2006: 1695.
Sloan WT, Lunn M, Woodcock S, Head IM, Nee S, Curtis TP. Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ Microbiol. 2006;8:732–40.
Keller A. Drosophila melanogaster’s history as a human commensal. Curr Biol. 2007;17:R77–81.
Corby-Harris V, Pontaroli AC, Shimkets LJ, Bennetzen JL, Habel KE, Promislow DEL. Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster. Appl Environ Microbiol. 2007;73:3470–9.
Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489:220–30.
Faust K, Raes J. Microbial interactions: from networks to models. Nat Rev Microbiol. 2012;10:538–50.
Berry D, Widder S. Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol. 2014;5:1–14.
Rivett DW, Scheuerl T, Culbert CT, Mombrikotb SB, Johnstone E, Barraclough TG, et al. Resource-dependent attenuation of species interactions during bacterial succession. ISME J. 2016;10:2259–68.
Morris BEL, Henneberger R, Huber H, Moissl-Eichinger C. Microbial syntrophy: interaction for the common good. FEMS Microbiol Rev. 2013;37:384–406.
Ponomarova O, Patil KR. Metabolic interactions in microbial communities: untangling the Gordian knot. Curr Opin Microbiol. 2015;27:37–44.
Zelezniak A, Andrejev S, Ponomarova O, Mende DR, Bork P, Patil KR. Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proc Natl Acad Sci USA. 2015;112:E7156.
Turroni F, Milani C, Duranti S, Mancabelli L, Mangifesta M, Viappiani A, et al. Deciphering bifidobacterial-mediated metabolic interactions and their impact on gut microbiota by a multi-omics approach. ISME J. 2016;10:1–13.
Rakoff-Nahoum S, Foster KR, Comstock LE. The evolution of cooperation within the gut microbiota. Nature. 2016;533:255–9.
Wong AC-N, Luo Y, Jing X, Franzenburg S, Bost A, Douglas AE. The host as the driver of the microbiota in the gut and external environment of Drosophila melanogaster. Appl Environ Microbiol. 2015;81:6232–40.
Blum JE, Fischer CN, Miles J, Handelsman J. Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster. mBio. 2013;4:e00860-13–e00860-13.
Dobson AJ, Chaston JM, Newell PD, Donahue L, Hermann SL, Sannino DR, et al. Host genetic determinants of microbiota-dependent nutrition revealed by genome-wide analysis of Drosophila melanogaster. Nat Commun. 2015;6:6312.
Agler MT, Ruhe J, Kroll S, Morhenn C, Kim S-T, Weigel D, et al. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol. 2016;14:e1002352.
Hajishengallis G, Darveau R, Curtis M. The keystone pathogen hypothesis. Nat Rev Microbiol. 2012;10:717–25.
Jordán F, Lauria M, Scotti M, Nguyen T-P, Praveen P, Morine M, et al. Diversity of key players in the microbial ecosystems of the human body. Sci Rep. 2015;5:15920.
Hoang D, Kopp A, Chandler JA. Interactions between Drosophila and its natural yeast symbionts - is Saccharomyces cerevisiae a good model for studying the fly-yeast relationship? PeerJ. 2015;3:e1116.
Stamps JA, Yang LH, Morales VM, Boundy-Mills KL. Drosophila regulate yeast density and increase yeast community similarity in a natural substrate. PLoS ONE. 2012;7:e42238.
Chandler JA, Eisen JA, Kopp A. Yeast communities of diverse Drosophila species: comparison of two symbiont groups in the same hosts. Appl Environ Microbiol. 2012;78:7327–36.
Huffnagle GB, Noverr MC. The emerging world of the fungal microbiome. Trends Microbiol. 2013;21:334–41.
Sam QH, Chang MW, Chai LYA. The fungal mycobiome and its interaction with gut bacteria in the host. Int J Mol Sci. 2017;18:330.
Chaston JM, Newell PD, Douglas AE. Metagenome-wide association of microbial determinants of host phenotype in Drosophila melanogaster. mBio. 2014;5:e01631–14.
Winans NJ, Walter A, Chouaia B, Chaston JC, Douglas AE, Newell PD. A genomic investigation of ecological differentiation between free-living and Drosophila-associated bacteria. Mol Ecol. 2017;26:4536–50.
Brady CL, et al. Transfer of Pantoea citrea, Pantoea punctata and Pantoea terrea to the genus Tatumella emend. as Tatumella citrea comb. nov., Tatumella punctata comb. nov. and Tatumella terrea comb. nov. and description of Tatumella morbirosei sp. nov. Int J Syst Evol Microbiol. 2010;60:484–94.
DeSantis TZ, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72(7):5069–72.
Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy. Appl Environ Microbiol. 2007;73(16):5261–7.
Acknowledgements
We thank John McMullen for assistance with fly collections and Vince Martinson for technical advice. This research was funded by NSF grant BIO1241099.
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Adair, K.L., Wilson, M., Bost, A. et al. Microbial community assembly in wild populations of the fruit fly Drosophila melanogaster. ISME J 12, 959–972 (2018). https://doi.org/10.1038/s41396-017-0020-x
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DOI: https://doi.org/10.1038/s41396-017-0020-x
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