A conceptual framework for the phylogenetically constrained assembly of microbial communities

Abstract

Microbial communities play essential and preponderant roles in all ecosystems. Understanding the rules that govern microbial community assembly will have a major impact on our ability to manage microbial ecosystems, positively impacting, for instance, human health and agriculture. Here, I present a phylogenetically constrained community assembly principle grounded on the well-supported facts that deterministic processes have a significant impact on microbial community assembly, that microbial communities show significant phylogenetic signal, and that microbial traits and ecological coherence are, to some extent, phylogenetically conserved. From these facts, I derive a few predictions which form the basis of the framework. Chief among them is the existence, within most microbial ecosystems, of phylogenetic core groups (PCGs), defined as discrete portions of the phylogeny of varying depth present in all instances of the given ecosystem, and related to specific niches whose occupancy requires a specific phylogenetically conserved set of traits. The predictions are supported by the recent literature, as well as by dedicated analyses. Integrating the effect of ecosystem patchiness, microbial social interactions, and scale sampling pitfalls takes us to a comprehensive community assembly model that recapitulates the characteristics most commonly observed in microbial communities. PCGs' identification is relatively straightforward using high-throughput 16S amplicon sequencing, and subsequent bioinformatic analysis of their phylogeny, estimated core pan-genome, and intra-group co-occurrence should provide valuable information on their ecophysiology and niche characteristics. Such a priori information for a significant portion of the community could be used to prime complementing analyses, boosting their usefulness. Thus, the use of the proposed framework could represent a leap forward in our understanding of microbial community assembly and function.

Keywords: 16S; Community assembly; Community ecology; Microbiome.

Fig. 1

A phylogenetically constrained assembly model

Fig. 2

Framework implementation towards an increased understanding of microbial ecosystems. a Phylogenetic sequence analysis identifies PCGs from the 16S community table (1). The framework predicts the existence of a number of phylo-niches in the ecosystem (2). Bioinformatic analysis using PCG phylogeny and genomic databases illuminates phylo-niche characteristics (3). b The use of community composition, PCG structure, genomic databases, and pylo-niche characteristics to prime complementing network analysis, metabolic, and individual-based models will translate into an unprecedented understanding of the ecosystem, illuminating patch niche structure, assembly rules, and function, as well as ecosystem patch structure