Abstract:

[Objective] The biogeobattery effect is widely observed in freshwater and marine environments. Previous studies have demonstrated that organic matter undergoes distinct transformation processes under the biogeobattery effect, which can substantially influence overall carbon turnover. As the most mobile and reactive fraction of organic matter in sediments, dissolved organic matter (DOM) is a major contributor to carbon turnover and plays a pivotal role in regulating contaminant fate through adsorption, complexation, photosensitization, and redox reactions, thereby profoundly influencing sediment ecological health. However, the transformation characteristics of DOM under the biogeobattery effect and the underlying mechanisms remain poorly understood, resulting in the limited knowledge of the ecological functions and carbon turnover processes in sediments associated with this widespread natural phenomenon. [Methods] In this study, we constructed a series of reactors to characterize DOM properties and elucidate the mechanisms driving DOM transformation in coastal sediments under the biogeobattery effect. Three experimental groups were established: coastal sediment-only reactors (CK) as the control group; reactors without an electrical connection between the sediment and overlying water (SO), representing the absence of a biogeobattery effect; and reactors with an electrical connection between the sediment and overlying water (SC), representing the formation of a biogeobattery system. [Results] During the 84-day operation period, the electric potential of sediments across all layers in the SC group ranged from −193 to 319 mV (vs. Ag/AgCl), which was consistently higher than that in the CK and SO groups (−335 to 162 mV and −321 to −15.1 mV, respectively). These results clearly demonstrate that the artificial biogeobattery effect increased sediment electric potential. Moreover, the maximum output voltage across a 100 Ω external resistor in the SC group was 57.3 mV, while the maximum mean self-potential of the sediment (with the water-sediment interface defined as zero potential) reached 93.9 mV. Compared with previous studies, the lower output voltage observed in the SC group suggests a relatively weaker biogeobattery effect in this study. Under this relatively weak biogeobattery effect, DOM consumption efficiencies in the CK, SO, and SC groups were 51.5% ± 19.3%, 37.1% ± 25.4%, and 36.4% ± 9.1%, respectively. These results suggest that the biogeobattery effect may, to some extent, reduce DOM loss and enhance carbon retention in coastal sediments. Fluorescence analysis identified three major components in all DOM samples: a long-wavelength humic-like component, a fulvic-acid-like component, and a tyrosine-like component. After 84 days of operation, the tyrosine-like component became the dominant contributor to DOM fluorescence in all sediment samples, accounting for 68.40%, 74.93%, 73.98%, and 75.92% of the total fluorescence intensity in the initial sediment (IS), CK, SO, and SC groups, respectively. These results indicate a transformation trend from long-wavelength humic-like and fulvic-acid-like components toward the tyrosine-like component in the CK, SO, and SC groups, with the most pronounced transformation observed in the SC group. Owing to the relatively high abundance of tyrosine-like components, DOM in the SC group exhibited the highest electron-transfer capacity, reaching (5.20 ± 0.27) mmol·g⁻¹, compared with (4.01 ± 0.36) and (3.70 ± 0.08) mmol·g⁻¹ in the CK and SO groups, respectively. This enhanced electron-transfer capacity may facilitate electron-transfer processes within the sediment under the biogeobattery effect. Further analysis revealed that the SC group exhibited the lowest Fe(II) concentration and Fe(II)/total Fe ratio, while the SO2− 4 concentration remained comparable to that in the initial sediment. These altered iron and sulfur redox states may have increased sediment electric potential and reshaped microbial community structure, thereby promoting DOM transformation under the biogeobattery effect. After 84 days of operation, Proteobacteria exhibited a high relative abundance in the anodic biofilms of both the SO and SC groups, particularly on the SC anode, where they accounted for 62.16% of the microbial community. The enrichment of Proteobacteria in anodic biofilms suggests that this phylum may include key electroactive microorganisms (EAMs) involved in establishing the artificial biogeobattery effect. Furthermore, Proteobacteria showed significant negative correlations with the long-wavelength humic-like component, fulvic-acid-like component, DOM concentration, and UV indices, while exhibiting a significant positive correlation with the tyrosine-like component. These relationships suggest that Proteobacteria may contribute to the degradation and transformation of humic-like and fulvic-acid-like components into tyrosine-like substances, potentially explaining their enrichment on the SC anode. Among the 18 dominant genera identified in this study, Bacillus, Paenisporosarcina, Acinetobacter, Romboutsia, and Microbulbifer exhibited significant differences in their distribution patterns among the experimental groups. Specifically, the relative abundance of Bacillus increased significantly in both sediments and anodic biofilms of the SO and SC groups compared with that in the initial sediment (IS). Paenisporosarcina and Acinetobacter were enriched in anodic biofilms, accounting for 1.19% and 56.13% of the microbial community in the SC group, respectively. Bacillus, which has been reported to participate in the synthesis of aromatic compounds, and Paenisporosarcina, which is associated with the degradation of protein-like substances, both showed significant positive correlations with DOM content. Moreover, the tyrosine-like component exhibited significant positive correlations with Bacillus, Paenisporosarcina, and Acinetobacter, suggesting that these genera, particularly Acinetobacter, may contribute to the production or transformation of tyrosine-like components, thereby enhancing the electron-transfer capacity of DOM under the biogeobattery effect. [Conclusion] Collectively, these results suggest that microbial community composition and relative abundance are governed by sediment environmental conditions, particularly the availability and characteristics of electron donors and acceptors. The interplay among these factors regulates sediment electric potential and ultimately determines the molecular composition and electrochemical properties of DOM. This study provides a foundation for advancing our understanding of the ecological functions of coastal sediments exhibiting the biogeobattery effect and establishes a scientific basis for developing strategies to regulate carbon turnover. However, the results of this study represent a preliminary investigation based on a single sampling time point. Future studies incorporating observations at multiple time points are needed to elucidate the temporal dynamics of the biogeobattery effect and associated DOM transformation processes, thereby enabling a more comprehensive understanding of the ecological functions and carbon cycling processes associated with this natural phenomenon in coastal sediments.

Key words: biogeobattery effect, dissolved organic matter, spectral characteristics, sediment electric potential, microbial community

摘要：

【目的】生物地球电池效应广泛存在于地表水和海洋生态系统中，但其对沉积物溶解性有机质（Dissolved organic matter，DOM）转化的影响尚缺乏系统认识。本文旨在阐明近岸海域沉积物中DOM在人工生物地球电池效应下的转化特征及其微生物驱动机制。【方法】通过外置电极构建了近岸海域沉积物人工生物地球电池，共运行84 d。运行期间监测体系输出电压和沉积物电位，分析DOM含量、荧光组分和电化学特性，以及沉积物与电极生物膜的微生物群落结构。【结果】运行期间，当外接100 Ω电阻时，该体系的最高输出电压为57.3 mV；沉积物的最大平均自电位（以水-沉积物界面处电位为零点）为93.9 mV。与已有研究相比，本体系的输出电压较低，生物地球电池效应相对较弱。在此弱效应下，DOM含量在84 d内基本保持不变，而无该效应体系中DOM含量明显下降，说明该人工体系有助于减缓近岸海域沉积物中的碳损失，增强碳保留能力。此外，在该效应下，DOM更倾向于转化为电子转移能力较强的类酪氨酸物质，使得人工生物地球电池中DOM的电子转移能力达（5.20 ± 0.27）mmol·g⁻¹，明显高于无生物地球电池效应体系的（4.01 ± 0.36）与（3.70 ± 0.08）mmol·g⁻¹，有利于沉积物中的电子传递过程。【结论】生物地球电池效应通过调控沉积物中电子供体和受体的利用模式，提高了沉积物电位，进而驱动微生物群落结构变化，从而塑造了DOM的组成与电化学特性。本研究为深入理解具有生物地球电池效应的沉积物生态功能提供了关键依据，并为基于该效应的碳循环调控策略奠定了科学基础。

关键词: 生物地球电池效应, 溶解性有机质, 光谱特征, 沉积物电位, 微生物群落