Generational Specific Recruitment of Arsenic- and Antimony-Reducing Microorganisms in Plant Root-Associated Niches for Adapting to Metalloid-Metal Pollution

Abstract

The recruitment of microorganisms by plants can enhance their adaptability to environmental stressors, but how root-associated niches recruit specific microorganisms for adapting to metalloid-metal contamination is not well-understood. This study investigated the generational recruitment of microorganisms in different root niches of <i>Vetiveria zizanioides</i> (<i>V. zizanioides</i>) under arsenic (As) and antimony (Sb) stress. The <i>V. zizanioides</i> was cultivated in As- and Sb-cocontaminated mine soils (MS) and artificial pollution soils (PS) over two generations in controlled conditions. The root-associated microbial communities were analyzed through 16S rRNA, <i>arsC</i>, and <i>aioA</i> gene amplicon and metagenomics sequencing. <i>V. zizanioides</i> accumulated higher As(III) and Sb(III) in its endosphere in MS in the second generation, while its physiological indices in MS were better than those observed in PS. SourceTracker analysis revealed that <i>V. zizanioides</i> in MS recruited As(V)- and Sb(V)-reducing microorganisms (e.g., <i>Sphingomonales</i> and <i>Rhodospirillaceae</i>) into the rhizoplane and endosphere. Metagenomics analysis further confirmed that these recruited microorganisms carrying genes encoding arsenate reductases with diverse carbohydrate degradation abilities were enriched in the rhizoplane and endosphere, suggesting their potential to reduce As(V) and Sb(V) and to decompose root exudates (e.g., xylan and starch). These findings reveal that <i>V. zizanioides</i> selectively recruits As- and Sb-reducing microorganisms to mitigate As-Sb cocontamination during the generational growth, providing insights into novel strategies for enhancing phytoremediation of metalloid-metal contaminants.