Community structure and metabolic potentials of keystone taxa and their associated bacteriophages within rice root endophytic microbiome in response to metal(loid)s contamination

Heavy metal (HM) contamination of agricultural products is of global environmental concern as it directly threatened the food safety. Plant-associated microbiome, particularly endophytic microbiome, hold the potential for mitigating HM stress as well as promoting plant growth. The metabolic potentials of the endophytes, especially those under the HM stresses, have not been well addressed. Rice, a major staple food worldwide, is more vulnerable to HM contamination compared to other crops and therefore requires special attentions. Therefore, this study selected rice as the target plants. Geochemical analysis and amplicon sequencing were combined to characterize the rice root endophytic bacterial communities and identify keystone taxa in two HM-contaminated rice fields. Metagenomic analysis was employed to investigate the metabolic potentials of these keystone taxa. Burkholderiales and Rhizobiales were identified as predominant keystone taxa. The metagenome-assembled genome (MAG)s associated with these keystone populations suggested that they possessed diverse genetic potentials related to metal resistance and transformation (e.g., As resistance and cycling, V reduction, Cr efflux and reduction), and plant growth promotion (nitrogen fixation, phosphate solubilization, oxidative stress resistance, indole-3-acetic acid, and siderophore production). Moreover, bacteriophages encoding auxiliary metabolism genes (AMGs) associated with the HM resistance as well as nitrogen and phosphate acquisition were identified, suggesting that these phages may contribute to these crucial biogeochemical processes within rice roots. The current findings revealed the beneficial roles of rice endophytic keystone taxa and their associated bacteriophages within HM-contaminated rice root endophytic microbiome, which may provide valuable insights on future applications of employing root microbiome for safety management of agriculture productions.