A ridge-to-reef ecosystem microbial census reveals environmental reservoirs for animal and plant microbiomes

Abstract

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.

Seasonality and longer-term development generate temporal dynamics in the Populus microbiome

“…It is now clear that plant microbiomes comprise a subset of microbial communities from the immediate surrounding environment ( 38 , 51 ), and previous work has advocated using unified community ecology frameworks (e.g., see references 52 , 53 ) to understand the ecological processes through which plant-associated subsets assemble from broader microbial species pools ( 40 , 54 ). Empirical tests of these frameworks suggest a complex mixture of ecological selection, drift, and dispersal structure plant microbiomes, and the climatic, host genetic, and edaphic drivers of selection vary considerably in their identity and relative importance among plant species and ecosystems ( 17 , 40 , 55 ). This context dependency has slowed the establishment of general principles to describe the assembly of the plant microbiome ( 50 ), which limits our ability to predict how microbiomes and their host plants will respond to environmental change ( 16 ) and manipulate the plant microbiome to improve agricultural production and sustainability ( 56 , 57 ).…”

Environmental microbes promote phenotypic plasticity inDrosophilareproduction and sleep behavior

“…The location contains multiple climate and habitat types, thus providing a wide array of environmental conditions and site-specific microbiome compositions. A microbiome survey of aquatic, terrestrial, and organismal features of the site was recently described (18). To generate the inoculant, newly collected wild male flies were transferred to YS-food vials and raised at 25 °C with 50% humidity under a 12: 12 hr day/ night cycle.…”

Holobiont Evolution: Population Theory for the Hologenome

“…The colonization takes place from environmental source pools (Yamashita et al . 2014, Nitschke 2015, Amend et al . 2022).…”

“…The model assumes that larval hosts are colonized at random by microbes according to a Poisson distribution (Ellis and M. Delbr ück 1939). The colonization takes place from environmental source pools (Yamashita et al 2014, Nitschke 2015, Amend et al 2022 In both cases the green microbes are selected and the brown ones are not. With collective inheritance the selected parents contribute their microbes to a collective from which the microbes are distributed into the larval hosts.…”