Divergent microbial community and functional dynamics in mangrove sediments along a polycyclic aromatic hydrocarbons (PAHs) gradient in China

Background: Mangrove ecosystems, despite their vital ecological and socioeconomic value, face escalating threats from anthropogenic disturbances, particularly the accumulation of persistent organic pollutants such as polycyclic aromatic hydrocarbons (PAHs). Understanding microbial responses to PAH contamination is crucial for developing effective bioremediation strategies. This study aimed to investigate PAH distribution, microbial community dynamics, and degradation mechanisms in mangrove sediments across Beihai and Zhangzhou, China, to inform targeted restoration efforts. Results: PAH concentrations in mangrove sediments varied significantly (395.49 vs 232.83 ng/g d. w.), with spatial heterogeneity driven by anthropogenic inputs, nutrient availability, and total organic carbon (TOC). High-PAH sediments (section M3) near pollution sources exhibited reduced microbial diversity but significant enrichment of hydrocarbon-degrading taxa, including Acinetobacter (7.84% in M3 vs 0.01% - 0.04% elsewhere), Mycobacterium , and Nocardioides , which collectively represented 46.5% of identified PAH degraders. Metagenomic profiling identified 565 KEGG orthologs (KOs) and 351 enzymes associated with PAH degradation, enabling the reconstruction of complete PAH degradation pathways from initial oxidation to mineralization, with ring-hydroxylating dioxygenases (RHDs) playing a pivotal role in initial oxidation. Notably, dominant PAH-degraders were also key producers of PAH-degrading enzymes and carbohydrate-active enzymes (CAZymes), particularly glycosyltransferases (GTs) and glycoside hydrolases (GHs), which facilitated co-metabolism and enhanced PAH degradation. Conclusions: This study elucidates the adaptive mechanisms of mangrove sediment microbiomes to PAH stress, highlighting the synergy between specialized degraders ( Acinetobacter , Mycobacterium , Nocardioides ), PAH-degrading enzymes, and CAZyme-mediated co-metabolism. These findings deepen our understanding of microbial adaptation to PAH stress and establish a framework for targeted bioremediation strategies, such as enzyme-enhanced solutions, to mitigate PAH pollution while preserving mangrove ecological functions. These insights are critical for balancing ecosystem health and anthropogenic pressures in coastal environments.