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Abstract Food webs govern interactions among organisms and drive energy fluxes within ecosystems. With an increasing appreciation for the role of symbiotic microbes in host metabolism and development, it is imperative to understand the extent to which microbes conform to, and potentially influence, canonical food web efficiencies and structures. Here, we investigate whether bacteria and their taxa and functional genes are compositionally nested within a simple model food web hierarchy, and the extent to which this is predicted by the trophic position of the host. Using shotgun and amplicon sequencing of discrete food web compartments within replicate tank bromeliads, we find that both taxonomy and function are compositionally nested and largely mirror the pyramid-shaped distribution of food webs. Further, nearly the entirety of bacterial taxa and functional genes associated with hosts are contained within host-independent environmental samples. Community composition of bacterial taxa did not significantly correlate with that of functional genes, indicating a high likelihood of functional redundancy. Whereas bacterial taxa were shaped by both location and trophic position of their host, functional genes were not spatially structured. Our work illustrates the advantages of applying food web ecology to predict patterns of overlapping microbiome composition among unrelated hosts and distinct habitats. Because bacterial symbionts are critical components of host metabolic potential, this result raises important questions about whether bacterial consortia are shaped by the same energetic constraints as hosts, and whether they play an active role in food web efficiency. 

Abstract The species area relationship is a classic ecological law describing the relationship between habitat increase and the number of species. Species area relationships are resoundingly positive across macrobes such as plants and animals, and emerge through non-exclusive stochastic and deterministic processes including changes in immigration and extinction, drift, and environmental heterogeneity. Due to unique attributes of the microbial lifestyle, they may not abide by similar rules as macrobes, especially when it comes to spatial scaling. We predict that host-associated microbiomes will exhibit shallower species area relationships than free-living microbiomes due to strong host filtering, and that the species area relationships of bacteria will be shallower than fungi due primarily to differences in dispersal ability. We test these predictions in a relatively simple field system where bromeliad phytotelmata comprise aquatic ecosystems that support invertebrates and environmental substrates such as detritus. Larger phytotelmata generate larger habitat islands for microbiomes allowing us to explicitly examine their species area relationships. We find that the species area relationships of free-living and host-associated microbiomes differ, as do those of microbiome members. By assessing the relationship between environmental conditions and richness, and measuring diversity across scales, we posit that these observed differences in species area relationships are owed to differences in realized niches and dispersal abilities among microbes. These findings highlight that the classic laws of biological spatial scaling do not necessarily accurately represent microbiomes, and that the influence of area on diversity appears to be more important for some microbiomes and microbes than others. 

Microbes are found in nearly every habitat and organism on the planet, where they are critical to host health, fitness, and metabolism. In most organisms, few microbes are inherited at birth; instead, acquiring microbiomes generally involves complicated interactions between the environment, hosts, and symbionts. Despite the criticality of microbiome acquisition, we know little about where hosts’ microbes reside when not in or on hosts of interest. Because microbes span a continuum ranging from generalists associating with multiple hosts and habitats to specialists with narrower host ranges, identifying potential sources of microbial diversity that can contribute to the microbiomes of unrelated hosts is a gap in our understanding of microbiome assembly. Microbial dispersal attenuates with distance, so identifying sources and sinks requires data from microbiomes that are contemporary and near enough for potential microbial transmission. Here, we characterize microbiomes across adjacent terrestrial and aquatic hosts and habitats throughout an entire watershed, showing that the most species-poor microbiomes are partial subsets of the most species-rich and that microbiomes of plants and animals are nested within those of their environments. Furthermore, we show that the host and habitat range of a microbe within a single ecosystem predicts its global distribution, a relationship with implications for global microbial assembly processes. Thus, the tendency for microbes to occupy multiple habitats and unrelated hosts enables persistent microbiomes, even when host populations are disjunct. Our whole-watershed census demonstrates how a nested distribution of microbes, following the trophic hierarchies of hosts, can shape microbial acquisition.