Marine Bacteria Mediated Multimetal Stress Alleviation in Mangrove Plants Through DNA repair and Plant Growth Promotion Mechanisms

Abstract

Mangrove ecosystems are threatened by heavy metal contamination from industrial discharge, and coastal urbanization. Metals such as Cr(VI) and Pb(II) impair mangrove physiology by disrupting nutrient uptake, and inducing oxidative stress. Marine bacteria play a crucial role in enhancing plant resilience through their metal-detoxifying and diverse plant growth-promoting (PGP) abilities. The comparative assessment of Bacillus velezensis DW2115 and Pseudomonas aeruginosa KL2101, isolated from the Bhitarkanika mangrove ecosystem in Odisha, India, revealed that both strains tolerated elevated concentrations of multimetal Cr(VI) and Pb(II) up to 500 ppm. Among them, B. velezensis DW2115 exhibited a more pronounced resistance to multimetal stress of Cr(VI) and Pb(II). This enhanced resilience was supported by an integrated stress-response system involving elevated antioxidant activity, activation of DNA mismatch repair to maintain genomic stability under metal-induced mutagenic pressure, and stringent response driven metabolic reprogramming. Confocal microscopy revealed maximum biofilm biomass by B. velezensis DW2115 (19.23 ± 0.48 µm3/µm2) at 300 ppm and by P. aeruginosa KL2101 (15.23 ± 0.25 µm3/µm2) at 200 ppm of multimetal. FESEM–EDX confirmed the accumulation of Cr(VI) and Pb(II) on the biofilm-EPS matrices of both strains. ATR-FTIR and 1H NMR analyses showed alterations in functional groups, while CD spectroscopy indicated a 43% and 55% increase in random coil content at 500 ppm in B. velezensis DW2115 and P. aeruginosa KL2101, respectively. Further, bacterial inoculation improved the height and vigor index of Avicennia marina L. despite multimetal stress. SEM micrographs confirmed successful root colonization, further validated by ERIC-PCR. The inoculated plants showed improved growth accompanied by a marked decline in multimetal accumulation, with B. velezensis DW2115 reducing multimetal levels in roots (14.21%), shoots (28.75%), and leaves (34.54%), and P. aeruginosa KL2101 decreasing them by 11.11%, 21.15%, and 28.24%, respectively. Additionally, inoculation with these bacterial strains resulted in an upregulation of antioxidant activity and a concomitant decrease in lipid peroxidation in the mangrove plants. These findings demonstrated that B. velezensis DW2115 and P. aeruginosa KL2101 hold substantial potential as bioinoculants for mitigating heavy metal stress and enhancing the growth and resilience of mangrove plants.