Seed-borne and environmental transmission mechanisms drive diverse heavy metal-resistant plant growth-promoting bacteria (PGPB) in rice

Heavy metal-resistant plant growth-promoting bacteria (PGPB) play a crucial role in mitigating heavy metal stress and reducing heavy metal accumulation in plants. However, the origins and transmission mechanisms of PGPB and their associated heavy metal resistance genes (MRGs) in plants remain unclear. To fill this knowledge gap, we collected rice and related environmental samples from heavy metal-contaminated paddy fields. The microbial DNA was recovered from these rice and environmental samples and then analyzed using shotgun metagenomics at the metagenome-assembled genomes (MAGs) level. As a result, 805 MRG-PGPB combinations were detected in rice tissues and related environments under heavy metal contamination conditions. Core MRG-PGPB combinations shared across seed-rice (42.46%) and environment-rice (13.34%) interfaces collectively constituted 55.80% of the detected combinations, demonstrating that environmental translocation and seed-borne vertical transmission jointly drive over half of MRG-PGPB colonization in rice systems. Subsequent source-tracking analysis indicated that PGPBs present in rice primarily originated from seeds, with a substantial proportion also attributed to translocation within rice tissues. Phylogenetic analysis of dominant MRGs further demonstrated the seed-borne vertical transmission of MRGs-PGPB, while simultaneously elucidating that MRGs harbored by PGPB in rice could also be acquired via horizontal gene transfer (HGT) from environmental or seed-borne MRG-PGPB, particularly from atmospheric microbes such as Methylophilus and Serratia. These findings provide valuable insights into harnessing PGPB to enhance rice resilience against heavy metal contamination, thereby contributing to improved food security and sustainable agricultural practices.