Community-level signatures of ecological succession in natural bacterial communities

Abstract

A central goal in microbial ecology is to simplify the extraordinary biodiversity that inhabits natural environments into ecologically coherent units. We present an integrative top-down analysis of over 700 bacterial communities sampled from water-filled beech tree-holes in the United Kingdom at distances between 100km, combining an analyses of community composition (16S rRNA sequencing) with assays of community functional capacity (exo-enzymatic activities, ATP production, CO2 dissipation and yield). The communities were grown in laboratory conditions in a complex growth medium, what allowed us to investigate the relationship between composition and function, excluding confounding environmental factors. We found a distance-decay trend in the similarity of the communities, and simulated data allowed us to reject the hypothesis that stochastic processes dominated the assembly of the communities, suggesting that niche effects prevailed. Consistent with this idea, clustering of communities lead us to identify six distinct community classes encompassing samples collected at often distant locations. Using structural equation modelling, we explored how functions were interrelated, demonstrating that a representative functional signature can be associated with each community class. We obtained a more mechanistic understanding of the classes using metagenomic predictions with PiCRUST. Notably, this approach allowed us to show that these classes contain distinct genetic repertoires reflecting community-level ecological strategies. We finally formulated an over-arching ecological hypothesis about how local conditions drive succession in these habitats. The ecological strategies resemble the classical distinction between r- and K-strategists and could be extrapolated to other systems, suggesting that a coarse grained picture of microbial ecological succession may be explained by relatively simple ecological mechanisms.