In aquatic ecosystems, sediments are not only the repository of nutrients and organic particles in water but also the nutrient source of the overlying water and are an important part of the aquatic environment (Søndergaard et al., 1999). Simple organic compounds such as carbohydrates, starches, and proteins in sediments are quickly decomposed by functional bacteria, but lignin and resin are resistant to microbial decomposition and are not easily oxidized (Zaki et al., 2015; Wang et al., 2019). Easily degradable organics are decomposed into small molecular organic matter or inorganic matter through a series of microbial catabolic activities, which participate in the biogeochemical cycle of the polyculture ecosystem, thereby affecting the entire aquaculture environment (Behera et al., 2022). Studies have shown that the degradable components in surface sediments can affect the dynamics and metabolism of bottom fauna (Grant and Hargrave, 1987; Dell'Anno et al., 2000), and the content of degradable parts in organic matter can also be used to evaluate the nutritional status of ecosystems (Dell'Anno et al., 2002; Pusceddu et al., 2003).

Sediment is the habitat of many farmed animals and is very important to the success of farming (Boyd, 1995). During the farming period, residual baits and feces are continuously accumulated in the sediment, which increases the organic matter content of the sediment (Liu et al., 2022). It was reported that approximately 40.44% of sedimentary organic matter in shellfish aquaculture ecosystems can be assimilated by benthic bait animals, but 59.56% of sedimentary organic matter still needs microbial transformation (Ji et al., 1998). The degradation of easily degradable organics in sediments involves various types of functional bacteria, such as proteolytic bacteria, cellulose-decomposing bacteria, and starch-decomposing bacteria (Prijambada et al., 2009; Artha et al., 2019). These functional bacteria can produce proteases, dehydrogenases, lipases, amylases, oxidases, decarboxylases, and other extracellular enzymes acting on organic matter. Through anaerobic or aerobic processes, a series of biochemical reactions occur to degrade organic matter gradually and ultimately convert it into inorganic elements that can be absorbed and utilized by phytoplankton and aquaculture animals (Pisarek and Grata, 2013; Gawas et al., 2019). For example, the amylase secreted by starch-degrading bacteria can decompose the insoluble starch in the sediment into soluble monosaccharides, which are further decomposed into CO₂ and participate in the carbon cycle at the water-air interface (Prijambada et al., 2009; Artha et al., 2019). Different types of functional bacteria secrete different extracellular enzymes to promote the degradation of easily degradable organic matter in sediment, which plays an important role in the circulation of biogenic elements in the aquaculture system.

Benthic shellfish change the physical properties of the sediment, such as its spatial heterogeneity, surface composition, particle size distribution, and porosity, by digging holes and via ventilation, excretion, and other biological disturbances (Thayer, 1979) and then affect the easily degradable organics in sediment and its related decomposing bacteria. In addition, benthic shellfish can also transfer particulate organic matter (POM) from water into the sediment in the form of feces or pseudofeces through the filtering effect (Newell, 2004). Sinonovacula constricta is a common zoobenthos species in coastal areas of China. It has a filter-feeding habit and is one of the important cultured shellfish in coastal areas of China (Chang, 2007). Studies have shown that the water transparency was greatly improved during the rapid growth of razor clam from June to October (Ren and Li, 2016), and the sediment organic matter content in the polyculture pond was significantly lower than that in the monoculture pond (He and Li, 2013). This is because S. constricta absorbs suspended organic substances from the upper water surface through its water pipe, improves water transparency, and reduces organic matter content in sediments (Tsuchiya and Kurihara, 1979; Lukwambe et al., 2018). When its distribution density is high, the ability of the population to remove organic matter in sediments is significantly strengthened (Tsuchiya and Kurihara, 1979; Lukwambe et al., 2018). However, there is a lack of research on the effect of filter-feeding shellfish in polyculture ecosystems on easily degradable organics, which thus needs further study. Based on the above understanding, four experimental ecosystems were established in this study: S. constricta was mixed into a Portunus trituberculatus–Marsupenaeus japonicus polyculture ecosystem at different densities to clarify the effects on the distribution and proportion of easily degradable organics in sediment and the changes in the number of easily degradable organics-degrading bacteria in different marine aquaculture ponds.

The results showed that protein was the main easily degradable organics in the sediment of the polyculture system, with an average content of 0.8%, followed by carbohydrates (0.2%) and lipids (0.1%). In the Chaohu Lake ecosystem, the composition of easily degradable organics in surface sediments is mainly carbohydrates, followed by proteins and lipids (He et al., 2016). There are significant differences between polyculture ecosystems and lakes, which may be related to sediment sources. In lake ecosystems, degradable organic compounds such as carbohydrates, proteins, and lipids mainly come from higher-plant residues, zooplankton, plant excreta, and corpses (Baldi et al., 2010; Zhang et al., 2017). Feeding feed is an important difference between polyculture ecosystems and other aquatic ecosystems. Feed is rich in protein, and feed residue settles into the bottom mud, increasing the content of protein in sediment. Therefore, the protein content of easily degraded organic matter is the highest in the polyculture system. In addition, the contents of various substances in sediments in the algae-type lake area of the Taihu Lake were higher than those in the pond aquaculture ecosystem, and their compositions were lipids (0.77%), carbohydrates (0.45%), and proteins (0.08%) (Qi et al., 2019). This may be related to the influence of breeding management measures in the artificial breeding system. Lake ecosystems usually have existed for several decades. A large amount of organic matter is deposited in the sediment environment, while mariculture ponds are dried and dredged every year. This management method leads to the exposure of a large amount of organic matter to the air and to oxidation, which results in the degradation of sediments.

Previous studies have shown that cultured shellfish can accelerate the sedimentation of various organic substances in water (Hatcher et al., 1994). At the same time, shellfish exert the filter-feeding effect of continuous organic matter assimilation, significantly reducing sediment organic matter accumulation. In this study, the order of organic matter content in sediments of all aquaculture systems was PM > PMB₁ > PMB₂ > PMB₃, showing that the organic matter content in the sediment of PMB₃, which had the highest S. constricta density, was the lowest, and was significantly lower than that in the other polyculture ecosystems. This shows that mixed culture of S. constricta, especially a high-density mixed culture, will affect the content of organic matter in the sediment. In the pond polyculture ecosystem, suspended particles such as residual bait, excrement of cultured animals, and plankton in water are the main sources of sediment organic matter. The higher the density of S. constricta is, the stronger the sediment purification effect of this filter-feeding shellfish on the environment will be, and thus the stronger the feeding ability of filter-feeding benthic animals on bacteria, particulate organic matter and attached animals and plants in water will be, resulting in a lower content of sediment organic matter in the high-density S. constricta mixed pond than that in the shrimp and crab mixed pond. In this study, the content of easily degraded organic matter was also affected by the mixed culture of S. constricta. The results showed that the content of carbohydrates, lipids, and proteins in the PMB₃ sediment was the lowest, which was significantly lower than that in the other polyculture ecosystems. This may be related to the content of organic matter in the sediment. The higher the density of S. constricta is, the stronger the sediment purification effect of this filter-feeding shellfish on the environment and the lower the organic matter content in the sediment will be, thus reducing the total content of carbohydrates, lipids, and proteins in sediment. In addition, the nutrients required for the survival of filter-feeding shellfish are mainly proteins, lipids, and carbohydrates. Therefore, the higher the density of S. constricta in mixed polyculture, the greater the demand for nutrients and sediment protein.

Bacterial communities in sediments could affect the transformation processes of organic matter, and the changes in organic matter composition in sediments could also in turn change the abundance and composition of bacterial communities (Judd et al., 2006). The results of the correlation analysis showed that different types of easily degradable organics were significantly positively correlated with their corresponding functional bacteria ( Table 1 ). Previous studies also found that the total number of bacteria in the sediment ecosystem was closely related to the concentration of organic matter, and the number was positively correlated with the change in organic matter content (Albertelli et al., 1999; Hjelm et al., 2004), which is consistent with the conclusion of this study. In the aquaculture ecosystem, with the extension of breeding time, organic matter is enriched at the bottom of the pond, creating a good living environment for bacteria and promoting their mass reproduction. Therefore, the availability of readily biodegradable organic sediments may determine the abundance of corresponding decomposing bacteria.

According to previous studies, the change in bacterial number in sediment was controlled by temperature (Garland and Mills, 1991), organic matter content in sediment (Classen et al., 2003; Xu et al., 2020), redox conditions in sediment (Muyzer et al., 1993), and feeding effects of small and large benthic animals (Sherysheva, 2021). In this study, the numbers of starch-degrading bacteria, glutin-degrading bacteria, and lipid-degrading bacteria were the smallest in PMB₃, followed by PMB₂ and PMB₁, indicating that the mixed culture of different densities of S.constricta in the breeding system had an effect on the number of functional bacteria in the sediment. With the increase in breeding density, the number of starch-decomposing bacteria, gelatin-decomposing bacteria, and lipid-decomposing bacteria in the sediment decreased. The higher density of S. constricta can reduce the accumulation of residual bait in the sediment through the filter-feeding effect so that the organic matter content in the sediment is reduced, thus reducing the energy supply of functional bacteria. In addition, the number of cellulose-degrading bacteria was the largest in all breeding systems, which may be related to the environment of the breeding ponds. During the farming period, Suaeda salsa and other cellulose-rich plants grew in the pond dam and the surrounding shallow water area. Their dead bodies were deposited on the surface of the sediment, which may have promoted the growth and reproduction of cellulose-decomposing bacteria. The number of cellulose-decomposing bacteria in sediment was the highest in the polyculture ecosystem, which may be related to the higher biomass of S. salsa in the shallow water around PMB₃.

Based on the data on the physical and chemical factors of sediment from Chai et al. (2022), it was found that temperature had no significant effect on the change in organic matter content in sediment, while Ladd et al. (1981) found that increasing temperature would accelerate the decomposition rate of soil organic matter, which is inconsistent with the conclusions of this study. This may be because the increase in sediment temperature affects the appetite of benthic organisms, making the residual bait accumulate, and the sedimentation rate of sediment is much larger than the decomposition rate of organic matter, resulting in the non-significant effect of temperature on the change in organic matter content. In addition, based on the sediment physical and chemical factor data of Chai et al. (2022), it was found that the pH value and redox potential of sediment were negatively correlated with the content of easily degraded organic matter in sediment and the number of starch-degrading bacteria, glutin-degrading bacteria, and lipid-degrading bacteria (see Table 2 ). The reason for this result may be that the accumulation of easily degradable organics in sediment leads to an increase in the number of corresponding functional bacteria, thus accelerating the decomposition rate of organic matter. During the decomposition process, oxidized inorganic substances act as electron acceptors and are continuously reduced, resulting in a decrease in the redox potential in the sediment (Lv et al., 2018), while the decomposition of organic matter also releases HCO₃ ^- and CO₂, resulting in a decrease in pH in the sediment (Shakir et al., 2016). Previous studies have found that the oxidation–reduction potential (ORP) value can be affected by the number or activity of bacteria (Senga et al., 2010; Bollag and Stotzky, 2021).

In this study, through the analysis and comparison of easily degradable organics and related functional bacteria in the sediments of different polyculture ecosystems, it was found that the composition of easily degradable organics in the sediments was different from that in other aquatic ecosystems. Protein was the dominant factor, followed by carbohydrates and lipids. Affected by the biological disturbance of Sinonovacula constricta, the content of organic matter and the number of bacteria in the sediment changed, thereby affecting pH and ORP in the sediment. The pH and ORP are important factors that reflect the changes in the number of easily degradable organics and related functional bacteria in the sediment. During the farming period, the contents of carbohydrates, lipids, and proteins in the sediment of polyculture system PMB₃ were the lowest, and the easily degradable organics in the sediment were significantly correlated with its corresponding functional bacteria. High-density S. constricta coculture could significantly reduce the contents of carbohydrates, lipids, and proteins in sediment and the number of starch-degrading bacteria, glutin-degrading bacteria, and lipid-degrading bacteria. This study confirmed that the mixed culture of S. constricta can affect the content and proportion of easily degradable organics in the sediment and provide a basis for understanding the influence of S. constricta mixed culture on the sediment environment of marine aquaculture ponds.

The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding author.

HL and XC: Investigation, Formal analysis, Writing-original draft. DZ: Conceptualization, Data curation, Formal analysis. WX: Visualization, Writing-reviewing, and editing. JH: Supervision, Funding acquisition, Writing-reviewing, and editing. All authors contributed to manuscript revision, read, and approved the submitted version.

This work was supported by the National Science Foundation of China (Grant No. 32002395, 32172993); the Basic public welfare program of Zhejiang Province (Grant No. LGN22C190005); the Major Agricultural Technology Cooperation Plan of Zhejiang Province (Grant No. 2020XTTGSC03); the science and technology project of Zhoushan City and Putuo District (Grant No. 2018C31078, 2020JH131); the planned project of Zhejiang Marine Fisheries Research Institute (HYS-CZ-202105, HYS-CZ-202209).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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