Phylogenetic constraints on host filtering drive bacterial assembly along the Pisum soil-root continuum

Abstract

Plant-microbiota ecological interactions are of growing interest for their pivotal role in plant fitness. However, the evolutionary forces shaping these associations and the evolutionary consequences for both partners remain challenging to address empirically. Plants act as ecosystem engineers that selectively filter bacterial communities, but whether evolutionary history predicts bacterial ecological responses to host influence, and whether the host's filtering capacity is itself phylogenetically constrained, remain unresolved. We characterized 827 bacterial communities along a soil-root continuum (bulk soil, rhizosphere, rhizoplane, root endosphere and nodule) in 24 Pisum genotypes reflecting the diversity of the genus. Using full-length 16S rRNA gene sequencing, we combined community ecology with phylogenetic analyses and functional gene prediction to assess how the evolutionary histories of both plants and bacteria drive their associations. We found that host filtering imposes increasing phylogenetic constraints along the soil-root continuum on the ecological responses of bacterial communities. Moreover, the strength of these phylogenetic constraints varies across Pisum genotypes, and itself exhibits a phylogenetic signal. Plant filtering capacity correlates with the predicted abundance of key plant growth-promoting functions, suggesting its potential adaptive value. We reveal that the ability to recruit specific closely related bacterial taxa is constrained by Pisum phylogeny. Altogether, our study provides an ecophylogenetic workflow for investigating eco-evolutionary processes of host-microbiota interactions and suggests reciprocal feedbacks through niche construction.