Abstract
BACKGROUND: In arid ecosystems, soil microorganisms experience prolonged drought and nutrient limitation, resulting in widespread dormancy and a decoupling between microbial presence and activity. The rhizosphere is a resource-rich microenvironment where plants, inputs may alleviate these constraints and regulate microbial metabolic states. However, it remains unclear whether root system effects in extreme environments reflect taxonomic turnover or the activation of dormant soil bacteria. Here, we investigated whether the rhizosphere-surrounding soil (RSS) of Pappostipa frigida, a dominant perennial grass of the Andean steppe of the Atacama Desert, reshapes soil bacterial communities primarily by promoting the activation of dormant taxa rather than by recruiting distinct bacterial populations, and how this process influences microbial diversity, activity, and functional potential. RESULTS: We employed a combination of soil physicochemical analyses, RNA/DNA metabarcoding, shotgun metagenomic sequencing and culture-based assays to compare bulk soil (BS) and RSS bacterial communities. The active bacterial community in the RSS exhibited significantly higher diversity and Shannon index than those in BS, whereas total (DNA-based) communities showed no significant differences between soil compartments. Taxonomic structure was primarily shaped by soil compartment rather than nucleic acid type, and active bacteria in the RSS showed a stronger correlation with total bacterial populations than those in the BS. Notably, 65% of putatively dormant bacterial taxa in BS were detected as active in RSS, and 75% were recoverable in culture. Additionally, 24% were members of PGP bacterial families. Functionally, the bacterial communities of the BS were enriched in sporulation genes, whereas active bacterial communities in the RSS showed higher abundances of genes associated with osmotic stress tolerance, siderophore synthesis, and resuscitation-promoting factors. CONCLUSIONS: Our results indicate that the root system of Pappostipa frigida functions as a localized hotspot of microbial activity in an extreme arid environment by promoting the activation of dormant members of the soil microbial seed bank rather than by recruiting distinct taxa. By integrating microbial activity, functional traits, and culturability, this study highlights the central role of plant-associated microenvironments in regulating microbial life-history strategies in drylands and provides a mechanistic framework for understanding plant-microbe interactions under chronic environmental stress.