SIP-metagenomics reveals key drivers of rhizospheric Benzo[a]pyrene bioremediation via bioaugmentation with indigenous soil microbes

• Published in: Environmental pollution (1987) Vol. 360; p. 124620
• Main Authors: Zhao, Xuan, Cheng, Xianghui, Cai, Xixi, Wang, Shuang, Li, Jibing, Dai, Yeliang, Jiang, Longfei, Luo, Chunling, Zhang, Gan
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 01-11-2024
• Subjects: benzo[a]pyrene degrader; Bioaugmentation; Indigenous soil microbes; Metagenomic; Rhizoremediation; Stable isotope probing (SIP); Stable isotope probing (SIP); Indigenous soil microbes; Bioaugmentation; Rhizoremediation; benzo[a]pyrene degrader; Metagenomic
• ISSN: 0269-7491; 1873-6424
• DOI: 10.1016/j.envpol.2024.124620

Rhizoremediation and bioaugmentation have proven effective in promoting benzo[a]pyrene (BaP) degradation in contaminated soils. However, the mechanism underlying bioaugmented rhizospheric BaP degradation with native microbes is poorly understood. In this study, an indigenous BaP degrader (Stenotrophomonas BaP-1) isolated from petroleum-contaminated soil was introduced into ryegrass rhizosphere to investigate the relationship between indigenous degraders and rhizospheric BaP degradation. Stable isotope probing and 16S rRNA gene amplicon sequencing subsequently revealed 15 BaP degraders, 8 of which were directly associated with BaP degradation including Bradyrhizobium and Streptomyces. Bioaugmentation with strain BaP-1 significantly enhanced rhizospheric BaP degradation and shaped the microbial community structure. A correlation of BaP degraders, BaP degradation efficiency, and functional genes identified active degraders and genes encoding polycyclic aromatic hydrocarbon-ring hydroxylating dioxygenase (PAH-RHD) genes as the primary drivers of rhizospheric BaP degradation. Furthermore, strain BaP-1 was shown to not only engage in BaP metabolism but also to increase the abundance of other BaP degraders and PAH-RHD genes, resulting in enhanced rhizospheric BaP degradation. Metagenomic and correlation analyses indicated a significant positive relationship between glyoxylate and dicarboxylate metabolism and BaP degradation, suggesting a role for these pathways in rhizospheric BaP biodegradation. By identifying BaP degraders and characterizing their metabolic characteristics within intricate microbial communities, our study offers valuable insights into the mechanisms of bioaugmented rhizoremediation with indigenous bacteria for high-molecular-weight PAHs in petroleum-contaminated soils.
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•Introduced strain boosts benzo[a]pyrene (BaP) degraders & functional gene abundance.•Introduced strain enhances rhizospheric BaP degradation, shapes microbial community.•First stable isotope probing-metagenomics for BaP bioaugmentation in rhizosphere.•Glyoxylate and dicarboxylate drive rhizospheric BaP biodegradation.•Novel identification of degraders linked to BaP degradation.