Multi-omics analysis of Stenotrophomonas maltophilia S-11 reveals its potential for Pb2+ bioremediation in contaminated soil

Akasha Farooq; Rida Kanwal; Kinza Bashir; Xianrui Tian; Yulan Chen; Dongyang Liu; Lingzi Zhang; Quanju Xiang; Ke Zhao; Xiumei Yu; Qiang Chen; Petri Penttinen; Yunfu Gu

doi:10.1016/j.jhazmat.2025.138867

Multi-omics analysis of Stenotrophomonas maltophilia S-11 reveals its potential for Pb²⁺ bioremediation in contaminated soil

J Hazard Mater. 2025 Jun 7:495:138867. doi: 10.1016/j.jhazmat.2025.138867. Online ahead of print.

Authors

Affiliations

¹ Department of Microbiology, College of Resources, Sichuan Agricultural University, Chengdu 611130, China.
² Department of Microbiology, College of Resources, Sichuan Agricultural University, Chengdu 611130, China. Electronic address: petri.penttinen@helsinki.fi.
³ Department of Microbiology, College of Resources, Sichuan Agricultural University, Chengdu 611130, China. Electronic address: guyf@sicau.edu.cn.

PMID: 40499424
DOI: 10.1016/j.jhazmat.2025.138867

Abstract

Lead (Pb²⁺) contamination in soil poses a significant environmental threat, but bioremediation using plant growth-promoting bacteria offers a sustainable solution. We evaluated the Pb²⁺ detoxification potential of Stenotrophomonas maltophilia strain S-11, isolated from the buckwheat rhizosphere. The strain exhibited high Pb²⁺ tolerance, with a minimum inhibitory concentration of 18 mM, along with a Pb²⁺ removal efficiency of 78.4 % (Q) and a biosorption capacity (q) of 383.5 mg g⁻¹ in aqueous media. Genomic analysis identified key genes involved in Pb²⁺ resistance, including those associated with oxidative stress responses and metal ion binding. Transcriptomic analysis revealed upregulation of metal-binding proteins, extracellular polymeric substances (EPS), NADH oxidoreductase, and membrane transporters under Pb²⁺ stress, indicating a dual detoxification and sequestration strategy. In a pot experiment, inoculation with strain S-11 increased buckwheat biomass and reduced Pb²⁺ accumulation in roots and shoots compared to the uninoculated control. Additionally, strain S-11 successfully colonized the rhizosphere microbial community and decreased bioavailable Pb²⁺ in contaminated soil. The findings demonstrate that Stenotrophomonas sp. S-11 is a promising candidate for sustainable Pb²⁺ remediation, providing genomic, enzymatic, and structural insights into heavy metal stress mitigation and soil reclamation. The strain employs a coordinated resistance strategy involving biosorption, active metal accumulation, electron transport chain (ETC) remodeling, metal sequestration, and upregulation of key metabolic pathways to maintain energy and nutrient homeostasis under Pb²⁺ stress. This multifaceted approach enhances its survival under Pb²⁺ contamination and strengthens its potential as an effective bioinoculant for bioremediation in heavy metal-contaminated environments.

Keywords: Buckwheat; Pb(2+) contamination; Plant growth promoting bacteria (PGPB); Soil reclamation; Stenotrophomonas maltophilia S-11.