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Common Structuring Principles of the Drosophila Melanogaster Microbiome on a Continental Scale and Between Host and Substrate

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Common Structuring Principles of the Drosophila Melanogaster Microbiome on a Continental Scale and Between Host and Substrate Environmental Microbiology Reports (2020) 12(2), 220–228 doi:10.1111/1758-2229.12826 Brief Report Common structuring principles of the Drosophila melanogaster microbiome on a continental scale and between host and substrate Yun Wang, 1,2 Martin Kapun, 1,3,4 Lena Waidele, 1,2 Introduction Sven Kuenzel,5 Alan O. Bergland 1,6 and Environmental factors and stochastic processes play Fabian Staubach 1,2* important roles in shaping microbiomes (Spor et al., 1The European Drosophila Population Genomics 2011; van Opstal and Bordenstein, 2015). Recent data Consortium (DrosEU). across a variety of hosts, including mammals and 2Department of Evolutionary Biology and Animal insects, suggest that environmental factors like host diet Ecology, Biology I, University of Freiburg, Freiburg im often have a dominant effect on microbiome composition Breisgau, Germany. (Chandler et al., 2011; Wu et al., 2011; Staubach et al., 3Department of Evolutionary Biology and Environmental 2013; Wang et al., 2014; Waidele et al., 2017; Rothschild Studies, University of Zürich, Zürich, Switzerland. 4Department of Cell and Developmental Biology, et al., 2018). In order to explain variation between Medical University of Vienna, Vienna, Austria. microbiomes from the same species, stochastic, ecologi- 5Max Planck Institute for Evolutionary Biology, Plön, cally neutral processes have moved into focus. These Germany. processes comprise ecological drift, dispersal and coloni- 6Department of Biology, University of Virginia, zation history. It appears plausible for diverse species Charlottesville, VA, USA. (Sieber et al., 2019), including Drosophila (Adair et al., 2018) that neutral processes dominate microbiome assembly. Summary The ability of D. melanogaster to shape its associated The relative importance of host control, environmental microbiome might be limited (Blum et al., 2013; Wong effects and stochasticity in the assemblage of host- et al., 2013). Instead, probabilistic processes contribute associated microbiomes is being debated. We to gut colonization (Obadia et al., 2017) and community analysed the microbiome among fly populations that structure in natural populations can be explained to a were sampled across Europe by the European Dro- large extent by neutral ecological mechanisms (Adair sophila Population Genomics Consortium (DrosEU). In et al., 2018). As in mammals and other organisms, envi- order to better understand the structuring principles ronmental factors, such as the time of collection (Adair of the natural D. melanogaster microbiome, we et al., 2018; Behrman et al., 2018) or diet (Chandler combined environmental data on climate and food- et al., 2011; Staubach et al., 2013; Erkosar et al., 2018; substrate with dense genomic data on host Wang and Staubach, 2018) have a strong effect on the populations and microbiome profiling. Food-substrate, Drosophila microbiome. temperature, and host population structure correlated On the other hand, D. melanogaster microbiome struc- with microbiome structure. Microbes, whose abun- ture is associated with host genotype (Unckless et al., dance was co-structured with host populations, also 2015; Chaston et al., 2016; Behrman et al., 2018), indi- differed in abundance between flies and their sub- cating at least low levels of genotype-dependent micro- strate in an independent survey. This finding suggests biome structuring. While the midgut and the stool of flies common, host-related structuring principles of the share many microbial taxa, they nonetheless differ signifi- microbiome on different spatial scales. cantly as has been shown by 16S rRNA gene sequenc- ing in Fink and colleagues, (2013), suggesting a selection process inside the fly takes place. Digestion of fl *For correspondence. E-mail [email protected]. bacteria, persistence and proliferation in the y gut could de; Tel. +49-761-203-2911. play a role in this process (Obadia et al., 2017; Inamine © 2020 The Authors. Environmental Microbiology Reports published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. European Drosophila microbiomes 221 et al., 2018). Wong and colleagues. (2015) showed that for the co-structure of the microbiome with host genetic flies affect their microbiome and that of their immediate variation (Fig. S1). From this data set, we identified bac- environment. Evidence that D. melanogaster exerts con- terial taxa that correlated with the host population struc- trol over its microbiome that goes beyond an effective ture. These taxa were analysed in an independent immune response comes from a recent study, which experiment, where we compared fly-associated found that D. melanogaster larvae foster beneficial Lacto- microbiomes to that of their substrate, to test for potential bacillus plantarum via excretions (Storelli et al., 2018). effects of host filtering at a small scale. Finally, we Pais and colleagues. (2018) showed that Acetobacter assessed the fitness effects from the recent literature of thailandicus can persist in the gut of D. melanogaster, those taxa that were filtered by the host. can be dispersed by the host and provide a fitness bene- fit to the host, while closely related Acetobacter strains cannot. In lab-reared flies, dysregulation of antimicrobial Results effectors leads to highly specific changes in microbiome We analysed a total of 5 217 762 16S rRNA reads after composition that can affect closely related taxa in oppos- rigorous quality filtering (Table S2). A total of 2 672 402 ing ways. The resulting microbiome can be detrimental Wolbachia sequences were removed. We grouped the for the host (Ryu et al., 2008), suggesting fine-tuned host sequences into 100% identity operational taxonomic units control. (OTUs) to resolve strain-level differences because the Taken together, the D. melanogaster microbiome is interaction with the fly host may differ for closely related strongly affected by the environment and by stochastic bacteria (Ryu et al., 2008; Pais et al., 2018). Composition effects. At the same time, highly specific host genotype- and diversity of the bacterial microbiome were compara- dependent interactions with the microbiome seem to be ble to those from previous studies (Fig. S2). Host genetic at work. This is consistent with newly developed models data are based on allele frequency estimates from that combine environmental effects and host feedback on ~20 000 small intronic SNPs in 48 pooled population the metacommunity (Adair and Douglas, 2017) with dis- samples [Fig. 1, Fig. S1, (Kapun et al., 2018)]. persal and colonization dynamics (Miller et al., 2018). What is currently missing to understand the role of environmental factors and the host in microbiome compo- The natural D. melanogaster bacterial microbiome is co- structured with host genetic differentiation on a sition in D. melanogaster is more information on continental scale populations and environmental factors on different eco- logical scales and under natural conditions. These are Bray–Curtis Dissimilarity between bacterial communities conditions where the interaction between the Drosophila increases with geographic distance (r =0.196,P=0.0015, host and its microbiome has evolved. Mantel test, Fig. 1) indicating geographic structuring of If host genetic factors were important for the natural microbial communities associated with D. melanogaster microbiome associated with D. melanogaster, we would on a continent-wide scale. Jaccard and Morisita-Horn dis- expect co-structure of host genetic variation with the tances provided almost identical results (Fig. S3). microbiome. Furthermore, we would expect that microbes When accounting for geographic distance, host genetic that are affected by host genetic factors should differ in distance still explained a significant proportion of the vari- abundance between the host and its environment ance (r = 0.19, P = 0.02, Partial Mantel test, Fig. S3). because the effects of host genetic variation on the Beta diversity was rather continuously distributed across microbiome should be smaller or absent outside the host. the European continent (Fig. S4A–C). Furthermore, we Finally, if the genetic variation present in natural did not detect any effects of the English Channel nor the populations evolved under selective pressure to preferen- Alps on beta diversity. tially associate with beneficial microbes those microbes enriched in the host should have a propensity to provide Host genetic differentiation, temperature and food- fitness benefits as opposed to detrimental bacteria. substrate correlate with microbiome structure In order to test these predictions, we profiled the micro- biome in 50 samples across Europe. Because the Dro- We modelled microbiome composition in a redundancy sophila microbiome is dominated by bacteria (Bost et al., analysis (RDA) framework. We selected temperature, 2018; Kapun et al., 2018), we used 16S rRNA gene precipitation and substrate as plausible (Chandler et al., sequencing (Fig. 1 and Table S1). The sampling range 2011; Staubach et al., 2013; Thompson et al., 2017; covered different climates and allowed us to address the Wang and Staubach, 2018) candidate external environ- effect of environmental factors on the microbiome. We mental variables that could affect microbiome structure. combined the 16S profiles with population-level allele fre- Because microbial communities
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