Root-associated functional microbiome endemism facilitates heavy metal resilience and nutrient poor adaptation in native plants under serpentine driven edaphic challenges.

Abstract

Serpentine soils are characterized by high concentrations of heavy metals (HMs) and limited essential nutrients with remarkable endemic plant diversity, yet the mechanisms enabling plant adaptation to thrive in such harsh environments remain largely unknown. Full-length 16S rRNA amplicon sequencing, coupled with physiological and functional assays, was used to explore root-associated bacterial community composition and their metabolic and ecological functions. The results revealed that serpentine plant species exhibited significantly higher metal transfer factor values compared to non-serpentine plant species, particularly evident in Bidens pilosa, Miscanthus floridulus, and Leucaena leucocephala. The serpentine root-associated microbes showed a higher utilization of carboxylic acid, whereas carbohydrate utilization was higher in the non-serpentine site. Zymomonas mobilis and Flavabacterium sp. exhibited high resistance to heavy metal concentrations, showing greater adaptability, while, Staphylococcus carnosus showed sensitivity to HMs, showing limited adaptability. Moreover, Ni, Cr, and Co resistance genes were found, while nitrogen and phosphorous metabolism genes were less abundant in the serpentine site compared to the non-serpentine site. Furthermore, Flavobacterium sp. had a strong positive relationship with Cd and Cu, Zymomonas mobilis with Ni, and Cr, Streptomyces sp. with Co, and Staphylococcus carnosus with N and P cycling. These findings underscore critical role of root-associated bacterial communities and distinctive soil conditions of serpentine habitats in fostering ecological adaptation of native plant species to the challenges posed by HMs and nutrient deficiencies.