Mineral substrates as evolutionary drivers of soil microbial diversity through the rare biosphere

ABSTRACT Minerals are fundamental yet underappreciated drivers of microbial ecology. Traditionally viewed as passive nutrient sources or inert scaffolds, their broader ecological roles remain poorly defined. This study investigates the evolutionary influence of substrates (minerals and rocks) on soil bacterial communities through serial passage evolution experiments. Soil-derived microbial consortia from three distinct locations were exposed to nutritive (olivine, granite, diorite) and non-nutritive (quartz, kaolinite, montmorillonite) substrates under nutrient-rich conditions to isolate substrate-specific effects. Results revealed systemic variations of community structure across all treatments, characterized by elevated Firmicutes / Bacteroidetes ratio and taxonomic changes predominantly driven by rare taxa. These discoveries indicate that, under the influence of substrates, the communities shifted toward ones that preferentially utilize more labile carbon. Crucially, the acute responsiveness of rare taxa to mineral-induced environmental selection suggests that, although abundant taxa appeared to maintain core community functions, the rare biosphere facilitated niche specialization and functional diversification. These findings position minerals as dynamic drivers of microbial ecology and evolution, highlighting the mineralosphere as a critical microhabitat where abiotic properties govern biodiversity, functional redundancy, and evolutionary innovation in soil ecosystems. IMPORTANCE Even under nutrient-rich conditions, non-nutritive and chemically inert minerals, exemplified by quartz, actively reshape microbial community assembly. Through controlled serial-passage experiments, we show that distinct substrates selectively enrich rare biosphere members that expand functional potential and seed adaptation, while dominant taxa sustain core processes. These results reveal that mineral surface properties and physical interfaces, rather than nutrient supply, govern microbial diversification and evolutionary trajectories. Accordingly, the mineralosphere emerges as a dynamic microhabitat where abiotic complexity regulates biodiversity, metabolism, and long-term community succession. This reframes minerals and rocks as active ecological and evolutionary agents, bridging geomicrobiology and evolutionary ecology, with implications for soil health, biogeochemical cycling, and the origin and maintenance of microbial diversity.