Electricity generation and dibenzothiophene biodegradation using a novel electroactive bacterium Lysinibacillus macroides AP in microbial fuel cells

Abstract

Polycyclic aromatic sulfur heterocycles, such as dibenzothiophene (DBT), and their alkylated derivatives are recognized as persistent and toxic contaminants that pose major risks to the environment and human health. Here, a novel electroactive gram-positive bacterium, Lysinibacillus macroides AP, was isolated and identified from a microbial fuel cell (MFC) powered by aromatic compounds. An electricity generation performance with a maximum discharge voltage of 424.59 mV and a power density of 420.95 mW m⁻² was obtained using L. macroides AP in an MFC fueled with sodium formate. An analysis of the extracellular electron transfer (EET) mechanism indicated that the endogenous redox mediators produced by L. macroides AP were not detected, but exogenous redox mediators such as thionine acetate and anthraquinone-2, 6-disulfonate could temporarily enhance EET. The characterization of biofilm morphology revealed a dense network of microbial nanowires on the cell surface of L. macroides AP; the abundance of these nanowires was positively correlated with the discharge efficiency of the MFC, suggesting that the nanowires generated by L. macroides AP cells were likely to promote EET. Additionally, effective bioelectricity generation and simultaneous DBT degradation were successfully achieved using L. macroides AP in MFCs, with a power density of 385.20 mW m⁻² and 88.72 % DBT removal. This is the first report on a novel ecological role of L. macroides AP as a gram-positive electroactive bacterium, emphasizing its potential applications in environmental remediation and energy recovery.

Keywords

Lysinibacillus macroides / Dibenzothiophene degradation / Nanowires / Extracellular electron transfer / Microbial fuel cells

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.

CRediT Authorship Contribution Statement

Zihan Huang: Writing - original draft, Validation, Investigation, Formal analysis, Data curation. Lei Zhang: Methodology, Investigation, Formal analysis, Data curation. Ting Cai: Investigation, Formal analysis. Ruijun Liu: Investigation, Data curation. Xiaoyan Qi: Visualization, Methodology. Xia Wang: Writing - review & editing, Supervision, Resources, Funding acquisition, Conceptualization.

Data Availability Statement

The data supporting the findings of this study are included in this published article as well as in the Supplementary Materials available online.

Acknowledgments

This work was supported by grants from National Natural Science Foundation of China (32070097 and 91951202), National Key Research and Development Program of China (2019YFA0904803). We thank Sen Wang of the Core Facilities for Life and Environmental Sciences, State Key laboratory of Microbial Technology of Shandong University for SEM analysis.

References

[1] A. Modak, P. Bhanja, M. Selvaraj, et al. Functionalized porous organic materials as efficient media for the adsorptive removal of Hg (II) ions Environ. Sci. Nano, 7 (2020), pp. 2887-2923, 10.1039/D0EN00714E

[2] L. Lyu, L. Zhang, Q. Wang, et al. Enhanced Fenton Catalytic Efficiency of γ-Cu-Al₂O₃ by σ-Cu²⁺-Ligand Complexes from Aromatic Pollutant Degradation Environ. Sci. Technol., 49 (2015), pp. 8639-8647, 10.1021/acs.est.5b00445

[3] A. Bahuguna, M.K. Lily, A. Munjal, et al. Desulfurization of dibenzothiophene (DBT) by a novel strain Lysinibacillus sphaericus DMT-7 isolated from diesel contaminated soil J. Environ. Sci., 23 (2011), pp. 975-982, 10.1016/S1001-0742(10)60504-9

[4] B. Han, G. Wang, A. Liu, et al. Characteristics and source analysis of polycyclic aromatic hydrocarbons in organisms and manure near Ardley Island, Antarctica Mar. Pollut. Bull., 188 (2023),Article 114577, 10.1016/j.marpolbul.2023.114577

[5] R. Lohmann, R. Gioia, K.C. Jones, et al. Organochlorine Pesticides and PAHs in the Surface Water and Atmosphere of the North Atlantic and Arctic Ocean Environ. Sci. Technol., 43 (2009), pp. 5633-5639, 10.1021/es901229k

[6] A.M. Wagner, A.J. Barker Distribution of polycyclic aromatic hydrocarbons (PAHs) from legacy spills at an Alaskan Arctic site underlain by permafrost Cold Reg. Sci. Technol., 158 (2019), pp. 154-165, 10.1016/j.coldregions.2018.11.012

[7] J.A. Field, A.J.M. Stams, M. Kato, et al. Enhanced biodegradation of aromatic pollutants in cocultures of anaerobic and aerobic bacterial consortia Antonie Van Leeuwenhoek, 67 (1995), pp. 47-77, 10.1007/BF00872195

[8] L. Li, C.C. Zhao, Q.Y. Liu, et al. The Study of Degradation Characteristics of Isolated Pseudomonas Sp. LKY-5 on Dibenzothiophene Adv. Mat. Res., 864-867 (2013), pp. 136-139, 10.4028/www.scientific.net/AMR.864-867.136

[9] M.N. Carvalho, M. da Motta, M. Benachour, et al. Evaluation of BTEX and phenol removal from aqueous solution by multi-solute adsorption onto smectite organoclay J. Hazard. Mater., 239-240 (2012), pp. 95-101, 10.1016/j.jhazmat.2012.07.057

[10] M.I. Konggidinata, B. Chao, Q. Lian, et al. Equilibrium, kinetic and thermodynamic studies for adsorption of BTEX onto Ordered Mesoporous Carbon (OMC) J. Hazard. Mater., 336 (2017), pp. 249-259, 10.1016/j.jhazmat.2017.04.073

[11] J. Cheng, Y. Li, L. Li, et al. Thiol-/thioether-functionalized porous organic polymers for simultaneous removal of mercury (II) ion and aromatic pollutants in water New J. Chem., 43 (2019), pp. 7683-7693, 10.1039/C9NJ01111K

[12] P. Ghosh, S. Mukherji Environmental contamination by heterocyclic Polynuclear aromatic hydrocarbons and their microbial degradation Bioresour. Technol., 341 (2021), Article 125860, 10.1016/j.biortech.2021.125860

[13] A.E. Mbachu, E.I. Chukwura, N.A. Mbachu Role of Microorganisms in the Degradation of Organic Pollutants: a Review Int. J. Energy Environ. Eng., 7 (2020), pp. 1-11, 10.13189/eee.2020.070101

[14] N. Das, P. Chandran Microbial Degradation of Petroleum Hydrocarbon Contaminants: An Overview Biotechnol. Res. Int., 2011 (2011), pp. 1-13, 10.4061/2011/941810

[15] X. Qi, H. Wang, X. Gao, et al. Efficient power recovery from aromatic compounds by a novel electroactive bacterium Pseudomonas putida B6- 2 in microbial fuel cells J. Environ. Chem. Eng., 10 (2022), Article 108536, 10.1016/j.jece.2022.108536

[16] B.E. Logan, K. Rabaey Conversion of Wastes into Bioelectricity and Chemicals by Using Microbial Electrochemical Technologies Science, 337 (1979) (2012), pp. 686-690, 10.1126/science.1217412

[17] B.E. Logan, B. Hamelers, R. Rozendal, et al. Microbial Fuel Cells: Methodology and Technology Environ. Sci. Technol., 40 (2006), pp. 5181-5192, 10.1021/es0605016

[18] H. Wang, X. Qi, L. Zhang, et al. Efficient bioelectricity generation and carbazole biodegradation using an electrochemically active bacterium Sphingobium yanoikuyae XLDN2-5 Chemosphere, 307 (2022), Article 135986, 10.1016/j.chemosphere.2022.135986

[19] J. Lu, T. Nakajima-Kambe, T. Shigeno, et al. Biodegradation of dibenzothiophene and 4,6-dimethyldibenzothiophene by Sphingomonas paucimobilis strain TZS-7 J. Biosci. Bioeng., 88 (1999), pp. 293-299, 10.1016/S1389-1723(00)80012-2

[20] P.G. Rout, A. Singh, S.K. Behera Insights into the Kinetics of the Microbial Degradation of Dibenzothiophene (DBT) by Acidithiobacillus ferrooxidans Geomicrobiol. J., 41 (2024), pp. 451-458, 10.1080/01490451.2023.2245378

[21] L.X. Chen, Y.D. Li, X.C. Tian, et al. Electron Transfer in Gram-Positive Electroactive Bacteria and Its Application Prog. Chem., 32 (2020), pp. 1557-1563, 10.7536/PC200207

[22] G.P. Hu, Y. Zhao, F.Q. Song, et al. Isolation, identification and cyfluthrin-degrading potential of a novel Lysinibacillus sphaericus strain, FLQ-11-1 Res. Microbiol., 165 (2014), pp. 110-118, 10.1016/j.resmic.2013.11.003

[23] O.C. Nwinyi, O.O. Amund Biodegradation of Selected Polycyclic Aromatic Hydrocarbons by Axenic Bacterial Species Belonging to the Genera Lysinibacillus and Paenibacillus, Iran J. Sci. Technol. Trans. Sci., 41 (2017), pp. 577-587, 10.1007/s40995-017-0291-0

[24] J.G . Holt Bergey’s Manual of Determinative Bacteriology (9th ed.), Williams & Wilkins, Baltimore (1994)

[25] A. Coorevits, A.E. Dinsdale, J. Heyrman, et al. Lysinibacillus macroides sp. nov., nom. Rev Int. J. Syst. Evol. Microbiol., 62 (Pt_5) (2012), pp. 1121-1127, 10.1099/ijs.0.027995-0

[26] N. Kim, Y. Choi, S. Jung, et al. Effect of initial carbon sources on the performance of microbial fuel cells containing Proteus vulgaris Biotechnol. Bioeng., 70 (2000), pp. 109-114, 10.1002/1097-0290(20001005)70:1<109::AID--BIT11>3.0.CO;2-M

[27] G. Kong, Y. Yang, Y. Luo, et al. Cysteine-Mediated Extracellular Electron Transfer of Lysinibacillus varians GY 32 Microbiol. Spectr., 10 (2022), 10.1128/spectrum.02798-22

[28] X. Liu, Z. Li, C. Zhang, et al. Enhancement of anaerobic degradation of petroleum hydrocarbons by electron intermediate: Performance and mechanism Bioresour. Technol., 295 (2020), Article 122305, 10.1016/j.biortech.2019.122305

[29] H. Deng, H. Xue, W. Zhong A Novel Exoelectrogenic Bacterium Phylogenetically Related to Clostridium sporogenes Isolated from Copper Contaminated Soil Electroanalysis, 29 (2017), pp. 1294-1300, 10.1002/elan.201600673

[30] N. Samsudeen, T.K. Radhakrishnan, M. Matheswaran Effect of isolated bacterial strains from distillery wastewater on power generation in microbial fuel cell Process Biochem, 51 (2016), pp. 1876-1884, 10.1016/j.procbio.2016.06.007

[31] O. Choi, T. Kim, H.M. Woo, et al. Electricity-driven metabolic shift through direct electron uptake by electroactive heterotroph Clostridiumpasteurianum Sci. Rep., 4 (2014), p. 6961, 10.1038/srep06961

[32] X. Liu, L. Shi, J.D. Gu Microbial electrocatalysis: Redox mediators responsible for extracellular electron transfer Biotechnol. Adv., 36 (2018), pp. 1815-1827, 10.1016/j.biotechadv.2018.07.001

[33] B. Lai, S. Yu, P.V. Bernhardt, et al. Anoxic metabolism and biochemical production in Pseudomonas putida F 1 driven by a bioelectrochemical system Biotechnol. Biofuels, 9 (2016), p. 39, 10.1186/s13068-016-0452-y

[34] Y.Y. Lee, T.G. Kim, K. Cho Enhancement of electricity production in a mediatorless air-cathode microbial fuel cell using Klebsiella sp. IR21 Bioprocess Biosyst. Eng., 39 (2016), pp. 1005-1014, 10.1007/s00449-016-1579-8

[35] O. Adelaja, T. Keshavarz, G. Kyazze Enhanced biodegradation of phenanthrene using different inoculum types in a microbial fuel cell Eng. Life Sci., 14 (2014), pp. 218-228, 10.1002/elsc.201300089

[36] E. Baranitharan, M.R. Khan, D.M.R. Prasad, et al. Effect of biofilm formation on the performance of microbial fuel cell for the treatment of palm oil mill effluent Bioprocess Biosyst. Eng., 38 (2015), pp. 15-24, 10.1007/s00449-014-1239-9

[37] S.M. Tan, S.A. Ong, L.N. Ho, et al. The reaction of wastewater treatment and power generation of single chamber microbial fuel cell against substrate concentration and anode distributions J. Environ. Health Sci. Eng., 18 (2020), pp. 793-807, 10.1007/s40201-020-00504-w