Elsevier

Water Research

Volume 240, 15 July 2023, 120097
Water Research

Electromotive force induced by dynamic magnetic field electrically polarized sediment to aggravate methane emission

https://doi.org/10.1016/j.watres.2023.120097Get rights and content

Highlights

  • Exposure to a dynamic magnetic field enhanced the bio-methanogenesis in sediment.

  • Dynamic magnetic field induced electromotive force in sediment as electrical signals.

  • Electromotive force polarized amide groups to improve the sediment electro-activity.

  • Polarized proteins benefited proton-coupled electron transfer in respiration chains.

  • Enhanced proton out-flow in respiration chains promoted methanogenesis in sediment.

Abstract

As a primary driving force of global methane production, methanogens like other living organisms are exposed to an environment filled with dynamic electromagnetic waves, which might induce electromotive force (EMF) to potentially influence the metabolism of methanogens. However, no reports have been found on the effects of the induced electromotive force on methane production. In this study, we found that exposure to a dynamic magnetic field enhanced bio-methanogenesis via the induced electromotive force. When exposed to a dynamic magnetic field with 0.20 to 0.40 mT of intensity, the methane emission of the sediments increased by 41.71%. The respiration of methanogens and bacteria was accelerated by the EMF, as the ratios of F420H2/F420 and NAD+/NADH of the sediment increased by 44.12% and 55.56%, respectively. The respiratory enzymes in respiration chains might be polarized with the EMF to accelerate the proton-coupled electron transfer to enhance microbial metabolism. Together with the enriched exoelectrogens and electrotrophic methanogens, as well as the increased sediment electro-activities, this study indicated that the EMF could enhance the electron exchange among extracellular respiratory microorganisms to increase the methane emission from sediments.

Introduction

Bio-methanation in anaerobic environments is a critical factor for ozone depletion and global warming (Mand and Metcalf 2019), as substantial quantities (ca. 370∼444 Tg CH4/year) of methane generated from microbial metabolism of organic matter escape into the atmosphere (Liu and Whitman 2008). In nature, the CO2-reducing pathway is the most universal metabolism pattern of bio-methanation (Thauer et al. 2008), in which hydrogen serves as a typical electron donator to provide the reducing power for the reduction of CO2 (termed hydrogenotrophic methanogenesis). Some methanogens (like Methanosarcina. Spp) were reported to conduct an electrotrophic respiration to directly accept electrons from external electron sources (such as the exoelectrogens or electrode) (Holmes et al. 2018), of which the electron transfer is 8.57 folds higher than the H2 diffusion-dependent methanogenesis (Storck et al. 2016). The respiration of electrotrophic methanogens has been reported to be deeply engaged in the global carbon cycle (Mand and Metcalf 2019).

Electrochemical methods have been extensively reported to strengthen methanogenesis in anaerobic treatment systems (Wang et al. 2022a). In a typical bio-electrochemical system (BES), exoelectrogens oxidize organic matter and donated the generated electrons to the anode, and the electrons are further transported to the cathode for the reduction of H+ or CO2. With the biocatalysis of methanogens in the cathode, methane can be produced from CO2 reduction. However, many reports have suggested that the cathodic reduction with the electrons from external circuit only contributed to a quite low proportion of increased methane production in methanogenesis-based BESs (Jiang et al. 2022, Zakaria and Ranjan Dhar, 2021). While the enrichment of electrotrophic methanogens and exoelectrogens (Ren et al. 2018, Zhao et al. 2015), the up-regulation of the respiration-related genes (Franks et al. 2010, Zakaria and Ranjan Dhar, 2021), and the increased conductivity and capacitance of the microbial aggregations (Wang et al. 2020) were frequently observed with electrical stimulations, which could strengthen the electron exchange among the microorganisms to increase methane production (Li et al. 2017).

The earth is a giant magnet with a magnetic field intensity ranging from 20 (at the equator) to 70 μT (at the poles), and the electromagnetic induction between an active microorganism and geomagnetic field can also produce the induced electromotive force (EMF, about 0.075 mV/m) across the cell of organisms (Laa et al. 2020). Although such EMF or the current generated in the earth's magnetic field is too small to be perceived, it has profound effects on the physiological activities of organisms (e.g., the direction sense of pigeons (Mouritsen 2018) and the large-scale migrations of sea turtles) (Lohmann 1991). At present, the increasing applications of electromagnetic techniques (e.g., power production and transmission, signal radiation, radio transmission, etc.) have caused more exposure to electromagnetic pollution (Lv et al. 2022, Mircea and Philip 2015, Taormina et al. 2018). For example, it was reported that the surface of an electric power transmission system and a submarine power cable could generate an induced EMF up to 5.0 mT (Laa et al. 2020). Such exposure to an artificial and natural magnetic field may lead to a critical influence on the organisms. However, the effects of EMF on cell respiration related to methane production have been rarely investigated until now.

We anticipated that the EMF generated by a dynamic magnetic field might function similarly to electrical stimulation to affect the electron transfer behaviors of microorganisms in sediments. Such effects could increase methane emission in nature areas with high magnetic intensity. To verify the above considerations, a simulated wetland was utilized in this study to investigate whether the EMF generated by the relative motions between microbes and magnetic minerals could increase the CH4 emission of sediments. Effects of EMF on electron transfer chains and cell respiration were also explored.

Section snippets

Substrates and inoculum

The sediment was taken from Dongping Lake (Taian, China). After drying, grinding, and sieving, the sediment was added to the serum bottles for activation with synthetic glucose-based wastewater (Tab. S1) for two weeks. The main characteristics of the sediment sludge are as follows: total chemical oxygen demand (TCOD), 40339.58±1147.74 mg/L (mean ± standard deviation, n=3. In this study, the numbers after the ‘±’ represented the standard deviations.); total polysaccharide, 432.83±35.53 mg/L;

Generation of EMF to promote methane production in wetland sediment

Effects of dynamic magnetic intensity on voltage generation were assessed in the simulated wetland sediment. Under the static magnetic field (0∼30 s), the voltage (the open circuit potential, OCP) between the two ends of the sediment-filled silicone tube was maintained at a background level (around-48.54 mV vs. Ag/AgCl) (Fig. 1). When the electromagnet rotated horizontally to form the dynamic magnetic field (30∼80 s), the dramatical fluctuations of OCP were detected, in which meant that the

Conclusion

In summary, the study presented here showed that with a dynamic magnetic field, the induced EMF could increase the methane emission of sediments by 41.71%. As an electrical stimulation, the EMF caused the polarization of amide groups in protein-like substances, which increased the electro-activities of the sediments to promote the electron exchange between exoelectrogens and electrotrophic methanogens. Notably, the polarized respiratory enzymes strengthened the proton motions (outflow) coupled

CRediT authorship contribution statement

Qilin Yu: Conceptualization, Writing – original draft, Data curation. Haohao Mao: Data curation. Zhiqiang Zhao: Conceptualization. Xie Quan: Conceptualization. Yaobin Zhang: Conceptualization, Funding acquisition.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

The authors acknowledge the financial support from the State Key Research & Development Plan (2021YFA1201703) and National Natural Scientific Foundation of China (51978122 and 22276024).

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