Poly-γ-glutamic acid chelates chromium (III) and copper (II), alleviating their toxicity in cucumber and affecting rhizosphere bacterial community assembly

Abstract

The accumulation of chromium (Cr) and copper (Cu) in soil during industrialization and modernization poses an extreme threat to crops. Poly-γ-glutamic acid (γ-PGA) has the potential to stabilize heavy metals in soil through chelation because of the numerous carboxyl groups in its side chain. The rhizosphere microbiome contributes to plant detoxification by participating in heavy metal passivation. However, it is still unclear whether γ-PGA can alleviate the toxicity of Cr and Cu to plants and whether this effect is associated with changes in the rhizosphere microbiome assembly. Here, we found that γ-PGA application significantly reduced the content of Cr or Cu in cucumber plants by 67.45%-86.77% and 94.67%-98.21, respectively, and alleviated the oxidative stress of Cr or Cu to plants. Moreover, γ-PGA significantly increased the biomass of cucumber fruits in the plot experiment by 13.5% and 25.3% under Cr and Cu stress, respectively. The content of Cr or Cu in the cucumber fruit was below limits of detection, in contrast to the 31.23 mg/kg Cr or 9.86 mg/kg Cu detected in the no-γ-PGA treatment. γ-PGA effectively chelated Cr and Cu in vitro, and less than 30% of their chelates were degraded in 20 weeks, suggesting the strong stability of these chelates. γ-PGA significantly altered the rhizosphere bacterial community composition of cucumber by enriching phyla Gemmatimonadota, Acidobacteriota and Firmicutes, and genera Gemmatimonas and Stenotrophomonas, which potentially involved in reducing the mobility of Cr and Cu in soils. Furthermore, γ-PGA significantly enriched taxa assigned to plant growth-promoting bacteria (PGPB). Together, our results suggest that γ-PGA can reduce the Cr and Cu contents in cucumber, and this process is strongly associated with the chelation capacity of γ-PGA and its effects on rhizosphere microbiome composition. These results highlight the exciting potential to use γ-PGA for the remediation of heavy metal-contaminated soils.