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Dispersal homogenizes communities via immigration even at low rates in a simplified synthetic bacterial metacommunity.

ABSTRACT: Selection and dispersal are ecological processes that have contrasting roles in the assembly of communities. Variable selection diversifies and strong dispersal homogenizes them. However, we do not know whether dispersal homogenizes communities directly via immigration or indirectly via weakening selection across habitats due to physical transfer of material, e.g., water mixing in aquatic ecosystems. Here we examine how dispersal homogenizes a simplified synthetic bacterial metacommunity, using a sequencing-independent approach based on flow cytometry and mathematical modeling. We show that dispersal homogenizes the metacommunity via immigration, not via weakening selection, and even when immigration is four times slower than growth. This finding challenges the current view that dispersal homogenizes communities only at high rates and explains why communities are homogeneous at small spatial scales. It also offers a benchmark for sequence-based studies in natural microbial communities where immigration rates can be inferred solely by using neutral models.

SUBMITTER: Fodelianakis S

PROVIDER: S-EPMC6428813 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Dispersal homogenizes communities via immigration even at low rates in a simplified synthetic bacterial metacommunity.

Fodelianakis Stilianos S Lorz Alexander A Valenzuela-Cuevas Adriana A Barozzi Alan A Booth Jenny Marie JM Daffonchio Daniele D

Nature communications 20190321 1

Selection and dispersal are ecological processes that have contrasting roles in the assembly of communities. Variable selection diversifies and strong dispersal homogenizes them. However, we do not know whether dispersal homogenizes communities directly via immigration or indirectly via weakening selection across habitats due to physical transfer of material, e.g., water mixing in aquatic ecosystems. Here we examine how dispersal homogenizes a simplified synthetic bacterial metacommunity, using ...[more]

PMID: 30899017

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Project description:The rate, timing, and mode of species dispersal is recognized as a key driver of the structure and function of communities of macroorganisms, and may be one ecological process that determines the diversity of microbiomes. Many previous studies have quantified the modes and mechanisms of bacterial motility using monocultures of a few model bacterial species. But most microbes live in multispecies microbial communities, where direct interactions between microbes may inhibit or facilitate dispersal through a number of physical (e.g., hydrodynamic) and biological (e.g., chemotaxis) mechanisms, which remain largely unexplored. Using cheese rinds as a model microbiome, we demonstrate that physical networks created by filamentous fungi can impact the extent of small-scale bacterial dispersal and can shape the composition of microbiomes. From the cheese rind of Saint Nectaire, we serendipitously observed the bacterium Serratia proteamaculans actively spreads on networks formed by the fungus Mucor. By experimentally recreating these pairwise interactions in the lab, we show that Serratia spreads on actively growing and previously established fungal networks. The extent of symbiotic dispersal is dependent on the fungal network: diffuse and fast-growing Mucor networks provide the greatest dispersal facilitation of the Serratia species, while dense and slow-growing Penicillium networks provide limited dispersal facilitation. Fungal-mediated dispersal occurs in closely related Serratia species isolated from other environments, suggesting that this bacterial-fungal interaction is widespread in nature. Both RNA-seq and transposon mutagenesis point to specific molecular mechanisms that play key roles in this bacterial-fungal interaction, including chitin utilization and flagellin biosynthesis. By manipulating the presence and type of fungal networks in multispecies communities, we provide the first evidence that fungal networks shape the composition of bacterial communities, with Mucor networks shifting experimental bacterial communities to complete dominance by motile Proteobacteria. Collectively, our work demonstrates that these strong biophysical interactions between bacterial and fungi can have community-level consequences and may be operating in many other microbiomes.

Project description:The positive relationship between habitat heterogeneity and species richness is a cornerstone of ecology. Recently, it was suggested that this relationship should be unimodal rather than linear due to a tradeoff between environmental heterogeneity and population sizes. Increased environmental heterogeneity will decrease effective habitat sizes, which in turn will increase the rate of local species extinctions. The occurrence of the unimodal richness-heterogeneity relationship at the habitat scale was confirmed in both empirical and theoretical studies. However, it is unclear whether it can occur at broader spatial scales, for meta-communities in diverse and patchy landscapes. Here, I used a spatially explicit meta-community model to quantify the roles of two species-level characteristics, niche width and immigration rates, on the type of the richness-heterogeneity relationship at the landscape scale. I found that both positive and unimodal richness-heterogeneity relationships can occur in meta-communities in patchy landscapes. The type of the relationship was affected by the interactions between inter-patch immigration rates and species' niche widths. Unimodal relationships were prominent in meta-communities comprising species with wide niches but low inter-patch immigration rates. In contrast, meta-communities consisting of species with narrow niches and high immigration rates exhibited positive relationships. Meta-communities comprising generalist species are therefore likely to exhibit unimodal richness-heterogeneity relationships as long as low immigration rates prevent rescue effects and patches are small. The richness-heterogeneity relationship at the landscape scale is dictated by species' niche widths and inter-patch immigration rates. These immigration rates, in turn, depend on the interaction between species dispersal capabilities and habitat connectivity, highlighting the roles of both species traits and landscape structure in generating the richness-heterogeneity relationship at the landscape scale.

Dataset Information

Dispersal homogenizes communities via immigration even at low rates in a simplified synthetic bacterial metacommunity.

Publications

Dispersal homogenizes communities via immigration even at low rates in a simplified synthetic bacterial metacommunity.

Similar Datasets

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