In recent times, alongside the elevation of living standards, there has been a shift in the public’s food preferences from mere sustenance to a focus on quality. Marine fisheries, as a vital source of premium protein for human consumption, have seen a surge in global marine fish production (Liu et al., 2017). With dwindling wild fish stocks and escalating demand for marine products, marine aquaculture has emerged as a dominant sector in animal food production, contributing to more than 17% of the worldwide output (Lidder and Sonnino, 2012). Intensive aquaculture models, particularly cage aquaculture, are recognized for their high yield and efficiency (Calado et al., 2021). Owing to the burgeoning need for aquatic products, this form of aquaculture has gained global traction (Rasheeda et al., 2017; Xie et al., 2020). As the foremost aquaculture nation, as the world’s most important aquaculture country, China faces major challenges in coastal cage farming, including spatial constraints and environmental issues (Xie et al., 2020; Zhao et al., 2020). However, the environmental repercussions of prolonged aquaculture are significant. Issues such as nitrogen accumulation, the proliferation of related metabolites, and the excessive discharge of aquaculture effluents have been implicated in the degradation of water quality and alterations in microbial community compositions (Piedrahita, 2003; Zhang et al., 2019; Dantas et al., 2020). Meanwhile，prolonged fishery activities can contribute to eutrophication, triggering the proliferation of phytoplankton and harmful algal blooms. This eutrophication has had devastating effects on aquaculture, leading to various health issues such as oxygen depletion and parasite outbreaks, particularly in enclosed or semi-enclosed bays (Troell et al., 1997, 2009; Abreu et al., 2011). Eutrophication is a process in which the nutrient content of a water body increases, leading to changes in the nutritional status of the water body within a certain range (Meyer-Reil and Köster, 2000). Marine eutrophication is mainly caused by the input of nutrients from land sources, so eutrophication generally occurs in shallow coastal seas and bays, especially in estuaries where rivers flow into the sea. Eutrophication in estuaries, bays, and coastal waters has become a prominent ecological environmental issue worldwide (Karlsson et al., 2008; Claussen et al., 2009; Håkanson and Bryhn, 2011). Eutrophication has a significant impact on the cycling of marine nutrients (C, N, P, S, etc.), water quality, biodiversity, and the overall health of the coastal marine ecosystem (Ruihua, 1999; Paerl et al., 2003). Bacteria with rapid growth rates, as important components of aquatic environments, can exhibit sensitive and rapid responses to subtle changes in the marine environment (including pollution, physicochemical properties, and biological environment) through their productivity and role in material cycling, thereby serving as indicators (Paerl et al., 2003).

Aquaculture, as a significant marine industry, contributes high-quality protein globally, a fact well-documented in scientific literature (Campbell and Pauly, 2013). Intensive research efforts focused on the impacts of these aquaculture practices on environmental microorganisms from aquaculture (Murphy and Riley, 1962; Song et al., 2009; Liu et al., 2015). A noteworthy study from 2015 at a Chinook salmon farm in New Zealand underscored the profound influence of organic enrichment on the composition of bacterial communities (Dowle et al., 2015). Further research by Zhang et al. (2019) revealed a variety of carbon fixation mechanisms, such as the Calvin–Benson–Bassham (CBB), the Wood–Ljungdahl (WL), and the 3-hydroxypropionate (3-HP) pathways, in the microbiomes of Penaeus vannamei in pond water, sediment, and effluent under different cultivation conditions. The study also highlighted active sulfur and phosphorus cycling processes during advanced stages of shrimp cultivation, in addition to common nitrification and sulfide oxidation activities. This research marked the first detailed examination of the microbial community’s structure, function, and ecological cycles in shrimp farming environments, with a focus on their interaction with environmental factors (Zhang et al., 2019). These findings emphasize that in aquaculture environments microorganisms play an essential role in the cycling of nutrients, transforming exogenous organisms, and balancing biogeochemical cycles of elements like carbon, nitrogen, phosphorus, and sulfur. These processes are vital for maintaining ecological balance and health (Bai et al., 2014; Md Zoqratt et al., 2018). While much of the existing research concentrates on pond and factory farming systems (Dowle et al., 2015; Zhang et al., 2019), studies on open aquaculture models, particularly those impacting the ocean, have been less frequent. Research on the eutrophication of seawater caused by aquaculture has mainly focused on the interaction between algae and nitrogen-phosphorus ratios (Song et al., 2009), with limited studies on the eutrophication of water bodies caused by aquaculture in relation to microorganisms.

For this research, the cage aquaculture region in Lingshui County, Hainan Province, was chosen as the focal study area. Samples from both cage aquaculture waters and adjacent non-aquaculture marine areas were collected for analysis. The objective was to investigate the effects of water eutrophication caused by aquaculture on microbial community compositions and functions.

The microbial diversity in aquatic systems is a vital measure of the environmental quality of aquaculture settings and the health status of aquatic animals (Dantas et al., 2020). It also plays a pivotal role in preserving the ecosystem functions of these environments. In our study, we segmented Lingshui Xincun Port into designated aquaculture and non-aquaculture zones. This division allowed us to conduct a comparative analysis of the variations in microbial diversity within seawater across these areas, encompassing a broad spectrum of microbial taxa. At same time, notable differences were observed between the physicochemical characteristics of the surface water samples collected from aquaculture and non-aquaculture zones (Table 1). Overall, aquaculture zones were more nutrient-rich than non-aquaculture zones. The dissolved inorganic nitrogen (DIN) and soluble reactive phosphorus (SRP) concentration were significantly higher in aquaculture zones than in non-aquaculture zones.

Eutrophication has a significant impact on the cycling of marine nutrients (C, N, P, S, etc.), water quality, biodiversity, and the overall health of coastal marine ecosystems (Ruihua, 1999; Paerl et al., 2003). Bacteria with rapid growth rates, as important components of aquatic environments, can exhibit sensitive and rapid responses to subtle changes in the marine environment (including pollution, physicochemical properties, and biological environment) through their productivity and role in nutrient cycling, thereby serving as indicators (Paerl et al., 2003). The metagenomic sequencing data in this study revealed that Proteobacteria is the predominant phylum across all the samples, aligning with findings from previously published research (Fan et al., 2003; Cardona et al., 2016). In the genus-level annotations, a notable variation in the abundance of species groups was observed between aquaculture and non-aquaculture areas. This disparity may be indicative of the distinct roles these microbial groups play in different environmental contexts (Fan et al., 2017). Analysis using STAMP (v2.0) found that only Candidatus Pelagibacter (1.58–28.03%, Supplementary Table S2) was higher in the WA samples than in the WUA in Alphaproteobacteria. Gammaproteobacteria, including Vibrio and Pseudoalteromonas, was higher in the WA samples than in the WUA samples. The Candidatus Pelagibacter are the most abundant heterotrophs in the oceans and are believed to play a major role in mineralizing marine dissolved organic carbon. Vibrio and Pseudoalteromonas have been proven to be closely associated with eutrophication of seawater. A study on P. donghaiense found that as P. donghaiense is primarily a photoautotrophic organism with carbon needs mostly fulfilled from uptake of inorganic carbon, the environmental factors regarded to be crucial to its overgrowth during the bloom events are presumably availability of nitrogen and phosphorus, as suggested by previous laboratory observations (Varkitzi et al., 2010; Anderson et al., 2012). Kim et al. (2021) found through their study on the co-proliferation of Vibrio spp. and dinoflagellates Prorocentrum during a spring algal bloom in the coastal East China Sea that there is a clear correlation between Vibrio and algal blooms.

It was found that various carbon metabolic pathways had a higher abundance in the aquaculture area, with particular attention to the pathways related to methane metabolism (methano- genesis and anaerobic oxidation of methane (AOM) pathways). And these pathway-related genes also show a significant negative correlation with dissolved oxygen (DO). Research on the eutrophication of Guanabara Bay in Brazil found that gene libraries based on PCR-DGGE analysis showed that the phylotypes of methanogenic archaea were consistent with the nutrient environment gradient of polluted water bodies. The phylotypes of methanogenic archaea found in anaerobic polluted water bodies and most undamaged water bodies were closely related to known types found in these environments, indicating that water pollution-induced eutrophication factors regulate the methanogenic archaea community (Vieira et al., 2007). Meyer-Reil and Köster (2000) also believe that eutrophic habitats lead to an increase in the population of sulfate-reducing bacteria, while highly anaerobic conditions are conducive to the growth and reproduction of methanogenic archaea, resulting in an increase in the population of methanogenic archaea (Jiang et al., 2009). Therefore, the decrease in redox potential of habitats caused by water eutrophication, the increase in the number of sulfate-reducing bacteria, and the corresponding increase in the number of methanogenic archaea under highly anaerobic conditions are observed.

Nitrogen fixation, anaerobic ammonia oxidation (anammox), and dissimilatory nitrate/nitrite reduction to ammonium (DNRA) are all more abundant in aquaculture areas compared to non-aquaculture areas. In marine surface waters, NO₃⁻ is typically the most abundant form of nitrogen due to its oxidizing conditions (Patey et al., 2008; Mo et al., 2020). Microbial reactions, such as denitrification, anaerobic ammonia oxidation (anammox), and dissimilatory nitrate/nitrite reduction to ammonium (DNRA), which are predominantly anaerobic, can occur during intermittent hypoxic conditions, such as nocturnal anoxic events during high-biomass algal blooms and periods of extensive biomass decay following the decline of algal blooms (Conley et al., 2011; Turner et al., 2015). These nitrogen transformation reactions mediated by microbes may impact the supply of nitrogen to phytoplankton by influencing nitrogen availability and speciation. Since nitrogen is often considered the limiting nutrient for algal growth during rapid blooms, and previous studies have shown that certain nitrogen species are preferred by Prorocentrum spp. over others, investigating these microbially mediated nitrogen transformations could enhance our understanding of bloom dynamics in the East China Sea (Fan et al., 2003; Heil et al., 2005; Varkitzi et al., 2010).

In the schematic diagram of sulfur metabolism element cycling, only the pathway of thiosulfate disproportionation is significantly more abundant in aquaculture areas compared to non-aquaculture areas. Analysis of key genes related to sulfur metabolism that show significant differences between aquaculture areas and non-aquaculture areas revealed enrichment of six genes in aquaculture areas, including genes encoding adenylylsulfate kinase (cysC), tetrathionate reductase (ttrC), sulfhydrogenase (hydD/B), thiosulfate reductase (phsA), anaerobic dimethyl sulfoxide reductase (dmsA). Sulfate-reducing bacteria are a group of bacteria that use sulfate as the terminal electron acceptor during the oxidation of organic matter, with the end products being H₂S or S₂⁻. They are widely distributed in anaerobic sedimentary environments ranging from low to high latitudes (Xuezheng, 2008; Singh et al., 2011). The presence of sulfate-reducing bacteria signifies the occurrence of anaerobic environments, and the population size of these bacteria to some extent reflects the degree of anaerobiosis. Water eutrophication can easily lead to the occurrence of anaerobic environments, and therefore, the population size of sulfate-reducing bacteria can to some extent indicate the level of water nutrient enrichment. Existing studies have shown that in general, the abundance of sulfate-reducing bacteria is negatively correlated with dissolved oxygen content and positively correlated with water nutrient enrichment (Kim et al., 2021).

In summary, the cage aquaculture activities in Lingshui Xincun Port have led to water eutrophication. As the water nutrient levels change, the community structure and function of bacteria also undergo significant changes. The functions of bacteria in the ecosystem also respond to the eutrophication of seawater. The productivity of planktonic bacteria increases with eutrophication, enzyme decomposition potential rises, anaerobic respiration and functional activities are enhanced simultaneously. Eutrophication significantly disrupts the normal functional activity of microorganisms.

In the research on the impact of water eutrophication on bacteria, China’s research still has a certain distance from the world level, and most studies focus on the biomass and productivity of bacteria in freshwater ecosystems and coastal areas. With the rapid development of marine aquaculture, especially cage aquaculture, the trend of water eutrophication caused by marine aquaculture is becoming more serious. This study on the impact of aquaculture-induced water eutrophication on planktonic bacteria provides a new perspective for the management and regulation of eutrophication in aquaculture. And the research provides a basis for environmental management and ecological restoration in eutrophic areas of aquaculture.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article/Supplementary material.

All animal-involving experiments of this study were approved by the Animal Care and Use Committee of College of Marine Sciences, South China Agricultural University, and all efforts were made to minimize suffering.

ZL: Data curation, Formal analysis, Writing – original draft, Writing – review & editing, Investigation, Validation, Visualization. PW: Software, Supervision, Writing – review & editing. JL: Software, Supervision, Writing – review & editing. XL: Software, Writing – review & editing. YZ: Resources, Writing – review & editing. XH: Writing – review & editing. XZ: Resources, Writing – review & editing. WL: Conceptualization, Writing – review & editing. QQ: Conceptualization, Writing – review & editing, Funding acquisition.