High phylogenetic turnover magnifies evolutionary relatedness along bacterial primary succession

Abstract

Current models of microbial primary succession postulate that stochasticity dominates the early stages of soil community assembly, generating phylogenetically random patterns that are lost as abiotic and biotic filters gain relevance. We hypothesized that, under severe environmental stress, abiotic filters may override stochasticity from early successional stages, inducing phylogenetic clustering due to the overrepresentation of stress-tolerant lineages. Clustering may be magnified towards more carbon-rich stages due to intensified biotic interactions based on the overrepresentation of competitive clades. We also hypothesized that different plant life forms, with their contrasting effects on soil conditions, might modulate the phylogenetic patterns across microbial succession. To test these hypotheses, we collected 106 soil samples along plant size gradients of 13 species belonging to 4 life forms (trees, shrubs, perennial grasses, and dwarf shrubs) in seven sites in Mediterranean drylands in SE Spain. Samples in each gradient were taken in open areas (antecedent situation), underneath seedlings, juveniles, and mature plant individuals. In all cases, we detected large levels of phylogenetic clustering across the succession indicating a negligible role of stochasticity. Plant and soil variables drove different processes along the succession: Clustering of shallow-divergent lineages intensified along with plant growth and enrichment in soil organics, whereas clustering of deep-divergent lineages varied across plant life forms based on their effect on soil moisture. During primary succession, phylogenetic turnover increased due to the progressive enrichment in large lineages that were composed of closely related organisms and phylogenetically distant to the initial communities. Our data help fine-tune current models of bacterial primary succession indicating that (1) environmental filters can override stochasticity from the early stages of primary succession and (2) large levels of phylogenetic turnover can concur with increased evolutionary relatedness across gradients of microbial community assembly. Shifts in phylogenetic patterns may critically influence key ecosystem functions, such as decomposition and biogeochemical cycling, driven by soil microbiota.