The ecological relevance of flagellar motility in soil bacterial communities

Abstract

Flagellar motility is a key bacterial trait as it allows bacteria to navigate their immediate surroundings. Not all bacteria are capable of flagellar motility, and the distribution of this trait, its ecological associations, and the life history strategies of flagellated taxa remain poorly characterized. We developed and validated a genome-based approach to infer the potential for flagellar motility across 12 bacterial phyla (26,192 genomes in total). The capacity for flagellar motility was associated with a higher prevalence of genes for carbohydrate metabolism and higher maximum potential growth rates, suggesting that flagellar motility is more prevalent in resource-rich environments due to the energetic costs associated with this trait. To test this hypothesis, we focused on soil bacterial communities, where flagellar motility is expected to be particularly important given the heterogeneous nature of the soil environment. We applied a method to infer the prevalence of flagellar motility in whole bacterial communities from metagenomic data, and quantified the prevalence of flagellar motility across 4 independent field studies that each captured putative gradients in soil carbon availability (148 metagenomes). As expected, we observed a positive relationship between the prevalence of bacterial flagellar motility and soil carbon availability in each of these datasets. Given that soil carbon availability is often correlated with other factors that could influence the prevalence of flagellar motility, we validated these observations using metagenomic data acquired from a soil incubation experiment where carbon availability was directly manipulated with glucose amendments, confirming that the prevalence of bacterial flagellar motility is consistently associated with soil carbon availability over other potential confounding factors. Flagellar motility is a fundamental phenotypic trait for bacterial adaptation to soil, defining life history strategies primarily associated with resource availability. More generally, this work highlights the value of combining genomic and metagenomic approaches to expand our understanding of microbial phenotypic traits and reveal their general environmental associations.