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Identifying biochemical aspects of the potentially toxic elements (PTEs) is of particular concern in mangrove ecosystems, Avicennia marina (Forssk.) Vierh., due to their importance as natural buffers in coastal areas. Nonetheless, the microbial community dynamics and potential scavenging responses of mangrove ecosystems to the phytotoxicity of PTEs remain questionable. This study assesses the ecological risk benchmarks of some PTEs, including aluminum (Al), boron (B), barium (Ba), cadmium (Cd), cobalt (Co), chromium (Cr), copper (Cu), iron (Fe), mercury (Hg), manganese (Mn), nickel (Ni), lead (Pb), and zinc (Zn), and their microbial responses in the bottom sediments of mangrove ecosystems along Egypt's Red Sea coast. In particular, we assessed the role of microbial metabolites in biochemical cycling of nutrients and scavenging against phytotoxicity hazards. We quantified a spectrum of ecological risk assessment indices, which suggested elevated levels of PTEs in sediment, particularly Cr, Hg, and Pb. Canonical correspondence analysis and generalized linear mixed effects models indicate that the spatial biodiversity of microbial taxa is impacted significantly by the physicochemical characteristics of sediments and concentrations of PTEs. Results demonstrate that the microbial communities and their metabolites exert a significant influence on organic matter (OM) decomposition and the biochemical cycling of phytoavailable nutrients including nitrogen (N), phosphorus (P), and potassium (K). Spatially, nitrogenase activities were higher (411.5 μmoL h−1 mL−1) in the southern sites of the Red Sea coast relative to the northern locations (93.8 μmoL h−1 mL−1). In contrast, higher concentrations of phytohormones, including indole-3-acetic acid (IAA) (61.5 mg mL−1) and gibberellins (534.2 mg mL−1), were more evident in northern sites. Siderophores correlated positively with Fe concentration in sediments and averaged 307.4 mg mL−1. Overall, these findings provide insights into the biochemical signals of PTEs contamination in hostile environments, contributing to a better understanding of the future prospects of PTEs bioremediation in contaminated coastal environments. [Display omitted] • Toxic elements showed a contamination hazard in mangrove ecosystems. • Chromium, mercury and lead exhibited values above the WHO permissible limits. • Vegetation patterns modulate biochemical dynamics of toxic elements in sediments. • Microbial diversity regulates biochemical cycling of nutrients. • Microbial metabolites showed scavenging effects against phytotoxicity hazards. [ABSTRACT FROM AUTHOR]