Unveiling the novel role of ryegrass rhizospheric metabolites in benzo[a]pyrene biodegradation

Xuan Zhao; Jibing Li; Dayi Zhang; Longfei Jiang; Yujie Wang; Beibei Hu; Shuang Wang; Yeliang Dai; Chunling Luo; Gan Zhang

doi:10.1016/j.envint.2023.108215

Unveiling the novel role of ryegrass rhizospheric metabolites in benzo[a]pyrene biodegradation

Environ Int. 2023 Oct:180:108215. doi: 10.1016/j.envint.2023.108215. Epub 2023 Sep 16.

Authors

Xuan Zhao¹, Jibing Li², Dayi Zhang³, Longfei Jiang⁴, Yujie Wang⁵, Beibei Hu⁵, Shuang Wang⁶, Yeliang Dai⁶, Chunling Luo⁷, Gan Zhang⁴

Affiliations

¹ State Key Laboratory of Organic Geochemistry and Guangdong Provincial Key Laboratory of Environmental Protection and Resources Utilization, Guangdong-Hong Kong-Macao Joint Laboratory for Environmental Pollution and Control, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China; College of Architecture and Civil Engineering, Kunming University, Kunming 650214, China; CAS Center for Excellence in Deep Earth Science, Guangzhou 510640, China; University of Chinese Academy of Sciences, Beijing 100039, China.
² State Key Laboratory of Organic Geochemistry and Guangdong Provincial Key Laboratory of Environmental Protection and Resources Utilization, Guangdong-Hong Kong-Macao Joint Laboratory for Environmental Pollution and Control, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China; CAS Center for Excellence in Deep Earth Science, Guangzhou 510640, China; University of Chinese Academy of Sciences, Beijing 100039, China. Electronic address: lijibing@gig.ac.cn.
³ College of New Energy and Environment, Jilin University, Changchun 130021, China.
⁴ State Key Laboratory of Organic Geochemistry and Guangdong Provincial Key Laboratory of Environmental Protection and Resources Utilization, Guangdong-Hong Kong-Macao Joint Laboratory for Environmental Pollution and Control, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China; CAS Center for Excellence in Deep Earth Science, Guangzhou 510640, China.
⁵ School of Environmental Science and Engineering, Guangdong University of Technology, Guangzhou 510006, China.
⁶ State Key Laboratory of Organic Geochemistry and Guangdong Provincial Key Laboratory of Environmental Protection and Resources Utilization, Guangdong-Hong Kong-Macao Joint Laboratory for Environmental Pollution and Control, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China; CAS Center for Excellence in Deep Earth Science, Guangzhou 510640, China; University of Chinese Academy of Sciences, Beijing 100039, China.
⁷ State Key Laboratory of Organic Geochemistry and Guangdong Provincial Key Laboratory of Environmental Protection and Resources Utilization, Guangdong-Hong Kong-Macao Joint Laboratory for Environmental Pollution and Control, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China; CAS Center for Excellence in Deep Earth Science, Guangzhou 510640, China. Electronic address: clluo@gig.ac.cn.

PMID: 37741005
DOI: 10.1016/j.envint.2023.108215

Abstract

Rhizoremediation is a promising remediation technology for the removal of soil persistent organic pollutants (POPs), especially benzo[a]pyrene (BaP). However, our understanding of the associations among rhizospheric soil metabolites, functional microorganisms, and POPs degradation in different plant growth stages is limited. We combined stable-isotope probing (SIP), high-throughput sequencing, and metabolomics to analyze changes in rhizospheric soil metabolites, functional microbes, and BaP biodegradation in the early growth stages (tillering, jointing) and later stage (booting) of ryegrass. Microbial community structures differed significantly among growth stages. Metabolisms such as benzenoids and carboxylic acids tended to be enriched in the early growth stage, while lipids and organic heterocyclic compounds dominated in the later stage. From SIP, eight BaP-degrading microbes were identified, and most of which such as Ilumatobacter and Singulisphaera were first linked with BaP biodegradation. Notably, the relationship between the differential metabolites and BaP degradation efficiency further suggested that BaP-degrading microbes might metabolize BaP directly to produce benzenoid metabolites (3-hydroxybenzo[a]pyrene), or utilize benzenoids (phyllodulcin) to stimulate the co-metabolism of BaP in early growth stage; some lipids and organic acids, e.g. 1-aminocyclopropane-1-carboxylic acid, might provide nutrients for the degraders to promote BaP metabolism in later stage. Accordingly, we determined that certain rhizospheric metabolites might regulate the rhizospheric microbial communities at different growth stages, and shift the composition and diversity of BaP-degrading bacteria, thereby enhancing in situ BaP degradation. Our study sheds light on POPs rhizoremediation mechanisms in petroleum-contaminated soils.

Keywords: Benzo[a]pyrene-degrading bacteria; Bioremediation; Metabolomics; Persistent organic pollutants degradation; Plant growth stages; Stable isotope probing (SIP).