Estuaries serve as the junction where rivers meet, making them particularly susceptible to the impacts of human activities and the pollutants that are released into the environment (Zeng et al., 2023). Changes in the physical and chemical properties of the water–sediment interface can lead to the re-release of pollutants into the external environment. This transition causes sediments to shift from functioning as a “sink” to becoming a “source” of contaminants, which can result in significant pollution in the estuary area and pose potential ecological risks (Grmasha et al., 2023).

Polycyclic Aromatic Hydrocarbons (PAHs) represent a significant category of persistent organic pollutants, primarily released through the combustion of fossil fuels, industrial discharges, and various anthropogenic activities (Xie et al., 2021). Sixteen PAHs have been identified as priority contaminants by the Environmental Protection Agency (EPA) of the United States (Bouzekry et al., 2024). Low molecular weight PAHs, which consist of 2–3 benzene rings, are classified as non-carcinogens. The high molecular weight PAHs, specifically those with 4 to 6 rings, are classified as carcinogens. Upon release into the environment, PAHs have the potential to migrate over considerable distances, dispersing into soils, sediments, water, and the atmosphere on a global scale (Dreij et al., 2019; Lv et al., 2020). The accumulation of PAHs in sediments over extended periods functions as a primary reservoir. Concentrations of PAHs in the Pearl River estuary and surrounding sea regions varied between 189 and 637 ng/g. The primary sources of pollution were identified as petroleum burning within the estuary and coal combustion in the areas beyond the estuary (Luo et al., 2006). The concentration of PAHs in the surface sediments of the estuarine region of the Pearl River Delta ranged from 69.1 to 1,297 ng/g, indicating a medium level of ecological risk (Li et al., 2021). Research has demonstrated that there is considerable spatial variability of PAHs in sediments between the northern and southern regions, attributed to differences in climate, energy sources, and industrial activities in China. PAHs are oleophilic and hydrophobic, allowing them to accumulate in the human body through inhalation, ingestion, and other routes. Their reputation as a major issue stems from the carcinogenic, mutagenic, and teratogenic impacts on aquatic organisms and human health (Han et al., 2022; Venkatraman et al., 2024). Consequently, recognizing their spatial distributions and assessing the ecological risks are essential for formulating management strategies that are customized to the areas.

The diversity of habitats and environments in estuarine regions, along with the numerous contaminants introduced by river inputs and sewage discharge, support microbial life and elicit varied responses to environmental stressors (Ohore et al., 2022; Qiang et al., 2021). Extended exposure to contamination can lead to the adaptation of certain microorganisms, resulting in alterations to the community structure. The microbial community plays a vital role in nutrient and organic matter cycling and constitutes a significant portion of biomass in sediments (Johnston and Leff, 2015). Previous research has shown that PAH pollution in sediments originating from industrial activities influences the composition and density of microbial communities, and can even disrupt their metabolic processes within the environment (Liu et al., 2018). Recent studies indicate a decrease in bacterial alpha-diversity in response to increased PAH concentrations, attributed to the proliferation of hydrocarbon-clastic organisms (Kimes et al., 2014; Jeanbille et al., 2016). Deltaproteobacteria and Gammaproteobacteria, known for their role in hydrocarbon degradation, are identified as the predominant and frequently occurring microbes in sediments located near coastal regions (Jeanbille et al., 2016). Nevertheless, the reaction of microorganisms to the persistent pollution of PAHs in sediment has not been comprehensively revealed, potentially due to the low concentration of PAHs and the intricate determination process involved. Recent findings indicate that chronic pollution extends exposure duration and enhances community stability, thereby promoting greater diversity within the bacterial community (Nogales et al., 2007; Zhang et al., 2008). Furthermore, it is suggested that environmental factors have a greater influence on microbial communities, indicating that the role of contaminants has been previously concealed and overlooked.

Jinzhou Bay represents a typical example of a heavily polluted coastal area in China, primarily attributed to the activities associated with nonferrous metal smelting industries. Significant quantities of metal(loid) and PAHs were discharged from the Huludao Zn Plant, recognized as one of the largest zinc facilities in Asia, into the estuarine and coastal regions (Li et al., 2012; Zeng et al., 2023). Investigation and analysis revealed that the concentration of PAHs was elevated in the sub-region. Therefore, it is essential to evaluate the occurrence and health risk of PAHs, as well as to identify the microbial community and its diversity in sediments, to comprehend the impacts of regional pollutant disturbances on estuarine ecosystems.

River and offshore estuarine sediments are major “sinks” for terrestrial pollutants. The levels of PAHs and the geochemical conditions at the sampling sites, ranging from the upstream of a contaminated river to the estuaries in offshore areas, were assessed and analyzed for comparison. The highest concentration of PAHs was detected at sewage outflows and near the Zn smelting plant, while the levels of PAHs in upstream locations were lower compared to those found in downstream estuaries at offshore sites. Previous study indicates that rivers serve as significant conduits, transporting land-derived sediments that contain contaminants, which can migrate and accumulate in estuarine sediments and offshore marine environments, leading to pollution of organic substances (Wu et al., 2022; Zeng et al., 2023). The levels of PAHs in estuarine sediments ranged from 1 to 251 ng/g, with a mean value of 50.38 ng/g observed in the marine sediments of the Mediterranean (Bouzekry et al., 2024). In contrast, the sediment from the Al-Hussainya River in Karbala Province, Iraq, exhibited concentrations from 0.36 to 119.06 μg/g dw (Hassan et al., 2019). Several sediment cores indicated the presence of PAH contamination “pockets,” displaying levels 200 times greater than those reported in the previous study, and comparable to the findings of the subsequent research. In the areas identified as “hot spots” for PAH-contaminated sediments, the predominant composition of PAHs consisted of three- and four-ring structures. Concentration of two-ring is relatively low primarily because the higher vapor pressure and greater water solubility of LMW PAHs, leading to more rapid volatilization or faster degradation rate (Lan et al., 2016; Murphy et al., 2016; Simo et al., 1997).

Different PAH sources exhibit distinct compositional patterns, and the isomer pair ratios analyzed in this study suggest that coal and fossil fuel combustion are likely the dominant contributors. Geospatial analysis revealed significantly higher PAH concentrations at site SD6 compared to other sampling locations. Given the absence of other high-energy-consuming industries or substantial domestic coal usage in the study area, emissions from the nearby Zn smelting plant are hypothesized to be the primary source of PAHs. This aligns with prior research identifying smelting operations as major emitters of industrial PAHs, often leading to significant PAH accumulation in adjacent soils (Boente et al., 2020). Furthermore, the predominance of 4-ring PAHs in the sediment profile supports their origin from high-temperature combustion processes (Mai et al., 2003), consistent with the industrial activities in the region. It has been reported that the sediments near the industrial area showed greater levels of PAHs than other sites, which may be attributed to variations in coal and fossil fuel combustion in adjacent areas (Zhang et al., 2023).

People living in coastal areas not only consume seafood such as clams directly, but also inevitably come into direct contact with pollutants in the sediment. Activities like fishing and recreational activities can all lead to the entry of these pollutants into the human body through various exposure routes, thereby posing health risks (Bouzekry et al., 2024). The cancer risk associated with PAHs for both children and adults was greater than that for adolescents. Children exhibit heightened sensitivity to environmental pollutants, attributed to their smaller body weight and skin surface area, which increases the likelihood of ingestion through frequent hand-to-mouth activities. Extended exposure to outdoor work or occupations may increase the potential cancer risk for adults (Halfadji et al., 2021). Furthermore, the contaminants present in the sediment are susceptible to influence and release from the surrounding environment, indicating that the associated health risks warrant careful consideration.

Hydrocarbon pollutants have been established as a key driver of microbial community composition and diversity shifts in marine sediments (Lin et al., 2023). Our findings align with Cheng et al. (2024), who reported Proteobacteria (20.6–80.0%) and Bacteroidetes (2.2–65.3%) as the dominant phyla in surface sediments. This phylogenetic distribution suggests that PAH contamination may selectively enrich hydrocarbon-degrading bacterial populations, thereby restructuring microbial communities. Notably, certain indigenous microbial taxa appear particularly adapted to PAH-stressed environments, as evidenced by increased functional gene transcripts and the proliferation of PAH-degrading specialists (Liu et al., 2021). The presence of Bacteroidetes, a phylum previously associated with hydrocarbon contamination in our study sites further supports this adaptive selection hypothesis (Haller et al., 2011). At the genus level, keystone species in our study were predominantly affiliated with Chloroflexi and δ-Proteobacteria. Anaerolineaceae, a family of Chloroflexi, widely distributed in anaerobic environments (e.g., sediments, wetlands, and wastewater systems) and demonstrated significant PAH degradation potential (Cheng et al., 2024). Within δ-Proteobacteria, the genus Desulfobulbus exhibited hydrocarbon degradation capacity under anaerobic conditions. Both Anaerolineaceae and Desulfuromonadales were closely associated with coupled carbon cycling and iron reduction processes across sediment layers, playing pivotal roles in organic matter mineralization (Coates et al., 2001). Previous studies indicated that Desulfobulbus and certain members of these groups are classified as sulfate-reducing bacteria (SRB), primarily resulting from anthropogenic activities (Cleary et al., 2012). Additionally, the class encompassing the majority of sulfate-reducing genera plays a vital role in the anaerobic breakdown of organic matter and is involved in the degradation of PAHs in sediments (Acosta-Gonzalez et al., 2013). Yan et al. (2018) denoted these species whose niche space might be relatively complementary, could respond to anthropogenic disturbances in the co-occurrence networks.

The co-occurrence of contaminants (e.g., PAHs) and key elements (e.g., C, N, P, and S) in sediments exerts complex influences on microbial community composition and function (Yang et al., 2020). RDA identified TOC, sulfur, TN, TP, and PAHs as key determinants shaping bacterial community structure. Notably, Xu et al. (2014) demonstrated that the coexistence of sulfur, nitrate and PAHs can enhance the abundance of functional genes in nitrate-reducing, sulfide-oxidizing bacteria and PAH-degrading microorganisms. Although PAHs are classified as persistent organic pollutants, they can also serve as carbon substrates for microbial metabolism (Cheng et al., 2024), potentially explaining the observed positive correlations between PAH concentrations and the relative abundance of certain microbial genera. Previous studies have well established the critical roles of carbon and phosphorus in governing microbial community structure (Zhang et al., 2023). Liu et al. (2021) further reported that elevated PAH levels, coupled with nitrogen and phosphorus enrichment in heavily polluted black-odor river sediments, may stimulate the growth of specific bacterial taxa and enrich functional genes associated with PAH degradation (nah, nidA) and sulfur reduction (dsrA). Additionally, Lapointe et al. (2005) have previously shown that sewage inputs are a primary source of nitrogen to marine harbor environments, while some sampling sites just located in the downstream area of the sewage discharge outlet. Such anthropogenic inputs can alter nitrogen and carbon cycling, thereby modulating the microbial community’s capacity to degrade pollutants (Atlas and Bartha, 1972; Murphy et al., 2016).

Elevated concentrations of PAHs in sedimentary pose significant ecological risks, potentially altering microbial community structure and impairing key biogeochemical cycling processes of carbon, nitrogen, phosphorus, and sulfur (Xu et al., 2014; Qian et al., 2021). However, current limitations in sequencing-based functional characterization hinder comprehensive understanding of microbial metabolic pathways, environmental adaptation mechanisms, and ecological roles under PAHs stress. Further investigations are warranted to elucidate these functional aspects at molecular level.

The present research provides a thorough assessment of the levels and ecological risks associated with PAHs, as well as an analysis of the community structure in sediments gathered from estuaries in offshore regions. The total PAH concentration in the sediment samples varied between 0.691 mg/kg and 25.083 mg/kg, and the TEQ_BaP values at each sample varied between 0.057 and 1.86 mg/kg, with approximately 30% of the sites surpassing ISQGs of the established standard. The greatest concentration of PAHs and associated health risks were identified at sewage outflow sites, with the highest cancer risk of PAHs were 2.41 × 10⁻⁵, 1.98 × 10⁻⁵, 3.04 × 10⁻⁵ for children, adolescents and adults, respectively. A comprehensive bacterial community was identified through phylogenetic analyzes, with the predominant groups being proteobacteria, bacteroidetes, and chloroflexi. PAH concentrations, in conjunction with sediment nutrient and geochemical parameters, were identified as key determinants shaping microbial community composition.