Electroactivity of the magnetotactic bacteria Magnetospirillum magneticum AMB-1 and Magnetospirillum gryphiswaldense MSR-1

Abstract

● The first study of electrochemically active magnetotactic bacteria.

● Two magnetotactic species are able to generate current in microbial fuel cells.

● Electron shuttle resazurin enables both species to reduce the crystalline Fe₂O₃.

● M. magneticum can reduce poorly crystalline iron oxide (FeOOH).

● Electroactivity might be common for magnetotactic bacteria.

Magnetotactic bacteria reside in sediments and stratified water columns. They are named after their ability to synthesize internal magnetic particles that allow them to align and swim along the Earth’s magnetic field lines. Here, we show that two magnetotactic species, Magnetospirillum magneticum strain AMB-1 and Magnetospirillum gryphiswaldense strain MSR-1, are electroactive. Both M. magneticum and M. gryphiswaldense were able to generate current in microbial fuel cells with maximum power densities of 27 and 11 µW/m², respectively. In the presence of the electron shuttle resazurin both species were able to reduce the crystalline iron oxide hematite (Fe₂O₃). In addition, M. magneticum could reduce poorly crystalline iron oxide (FeOOH). Our study adds M. magneticum and M. gryphiswaldense to the growing list of known electroactive bacteria, and implies that electroactivity might be common for bacteria within the Magnetospirillum genus.

Graphical abstract

Keywords

Magnetotactic bacteria / Magnetospirillum magneticum / Magnetospirillum gryphiswaldense / Extracellular electron transfer / Microbial fuel cells

References

[1] Amor M, Mathon F P, Monteil C L, Busigny V, Lefevre C T. (2020). Iron-biomineralizing organelle in magnetotactic bacteria: function, synthesis and preservation in ancient rock samples. Environmental Microbiology, 22(9): 3611–3632

[2] Coursolle D, Baron D B, Bond D R, Gralnick J A. (2010). The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis. Journal of Bacteriology, 192(2): 467–474

[3] Fathey R, Gomaa O M, Ali A E H, El Kareem H A, Zaid M A. (2016). Neutral red as a mediator for the enhancement of electricity production using a domestic wastewater double chamber microbial fuel cell. Annals of Microbiology, 66(2): 695–702

[4] Fernando E Y, Keshavarz T, Kyazze G. (2019). The use of bioelectrochemical systems in environmental remediation of xenobiotics: a review. Journal of Chemical Technology and Biotechnology, 94(7): 2070–2080

[5] Fessler M, Madsen J S, Zhang Y. (2022). Microbial interactions in electroactive biofilms for environmental engineering applications: a role for nonexoelectrogens. Environmental Science & Technology, 56(22): 15273–15279

[6] Fessler M, Madsen J S, Zhang Y. (2023). Conjugative plasmids inhibit extracellular electron transfer in Geobacter sulfurreducens. Frontiers in Microbiology, 14: 1150091

[7] Filman D J, Marino S F, Ward J E, Yang L, Mester Z, Bullitt E, Lovley D R, Strauss M. (2019). Cryo-EM reveals the structural basis of long-range electron transport in a cytochrome-based bacterial nanowire. Communications Biology, 2(1): 219

[8] Glasser N R, Saunders S H, Newman D K. (2017). The colorful world of extracellular electron shuttles. Annual Review of Microbiology, 71(1): 731–751

[9] Gu Y, Srikanth V, Salazar-Morales A I, Jain R, O’Brien J P, Yi S M, Soni R K, Samatey F A, Yalcin S E, Malvankar N S. (2021). Structure of Geobacter pili reveals secretory rather than nanowire behaviour. Nature, 597(7876): 430–434

[10] Hirose A, Kasai T, Aoki M, Umemura T, Watanabe K, Kouzuma A. (2018). Electrochemically active bacteria sense electrode potentials for regulating catabolic pathways. Nature Communications, 9(1): 1083

[11] Holmes D E, Dang Y, Walker D J F, Lovley D R. (2016). The electrically conductive pili of Geobacter species are a recently evolved feature for extracellular electron transfer. Microbial Genomics, 2(8): e000072

[12] Jiang Z, Liu Q, Dekkers M J, Barron V, Torrent J, Roberts A P. (2016). Control of Earth-like magnetic fields on the transformation of ferrihydrite to hematite and goethite. Scientific Reports, 6(1): 30395

[13] KochC, Harnisch F (2016). Is there a specific ecological niche for electroactive microorganisms? ChemElectroChem, 3(9): 1282–1295 10.1002/celc.201600079

[14] Lanas V, Logan B E. (2013). Evaluation of multi-brush anode systems in microbial fuel cells. Bioresource Technology, 148: 379–385

[15] Le NagardL, Morillo-López V, FradinC, BazylinskiD A (2018). Growing magnetotactic bacteria of the genus magnetospirillum: strains MSR-1, AMB-1 and MS-1. Journal of Visualized Experiments: JoVE

[16] Lefèvre C T, Bennet M, Landau L, Vach P, Pignol D, Bazylinski D A, Frankel R B, Klumpp S, Faivre D. (2014). Diversity of magneto-aerotactic behaviors and oxygen sensing mechanisms in cultured magnetotactic bacteria. Biophysical Journal, 107(2): 527–538

[17] LevarC E, Hoffman C L, DunsheeA J, TonerB M, BondD R (2017). Redox potential as a master variable controlling pathways of metal reduction by Geobacter sulfurreducens. bioRxiv 043059; doi: https://doi.org/10.1101/043059

[18] Li M, Yu X L, Li Y W, Han W, Yu P F, Lun Yeung K, Mo C H, Zhou S Q. (2022). Investigating the electron shuttling characteristics of resazurin in enhancing bio-electricity generation in microbial fuel cell. Chemical Engineering Journal, 428: 130924

[19] LiS L,Wang Y J,Chen Y C, Liu S M,Yu C P (2019). Chemical characteristics of electron shuttles affect extracellular electron transfer: shewanella decolorationis NTOU1 simultaneously exploiting acetate and mediators. Frontiers in Microbiology, 10.

[20] Lin W, Zhang W, Zhao X, Roberts A P, Paterson G A, Bazylinski D A, Pan Y. (2018). Genomic expansion of magnetotactic bacteria reveals an early common origin of magnetotaxis with lineage-specific evolution. ISME Journal, 12(6): 1508–1519

[21] Logan B E, Rossi R, Ragab A, Saikaly P E. (2019). Electroactive microorganisms in bioelectrochemical systems. Nature Reviews. Microbiology, 17(5): 307–319

[22] Lovley D R, Phillips E J. (1986). Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Applied and Environmental Microbiology, 51(4): 683–689

[23] Lovley D R, Walker D J F. (2019). Geobacter protein nanowires. Frontiers in Microbiology, 10: 2078

[24] Marsili E, Baron D B, Shikhare I D, Coursolle D, Gralnick J A, Bond D R. (2008). Shewanella secretes flavins that mediate extracellular electron transfer. Proceedings of the National Academy of Sciences of the United States of America, 105(10): 3968–3973

[25] Matsunaga T, Okamura Y, Fukuda Y, Wahyudi A T, Murase Y, Takeyama H. (2005). Complete genome sequence of the facultative anaerobic magnetotactic bacterium Magnetospirillum sp. strain AMB-1. DNA research: an international journal for rapid publication of reports on genes and genomes, 12: 157–166

[26] Matsunaga T, Sakaguchi T, Tadakoro F. (1991). Magnetite formation by a magnetic bacterium capable of growing aerobically. Applied Microbiology and Biotechnology, 35(5): 651–655

[27] Moisescu C, Ardelean I, Benning L. (2014). The effect and role of environmental conditions on magnetosome synthesis. Frontiers in Microbiology, 5(49): 1–12

[28] Reguera G, McCarthy K D, Mehta T, Nicoll J S, Tuominen M T, Lovley D R. (2005). Extracellular electron transfer via microbial nanowires. Nature, 435(7045): 1098–1101

[29] Schüler D, Köhler M. (1992). The isolation of a new magnetic spirillum. Zentralblatt für Mikrobiologie, 147(1–2): 150–151

[30] Smit B A, Van Zyl E, Joubert J J, Meyer W, Prévéral S, Lefèvre C T, Venter S N. (2018). Magnetotactic bacteria used to generate electricity based on Faraday’s law of electromagnetic induction. Letters in Applied Microbiology, 66(5): 362–367

[31] Straub K L, Benz M, Schink B. (2001). Iron metabolism in anoxic environments at near neutral pH. FEMS Microbiology Ecology, 34(3): 181–186

[32] StookeyL L (1970). Ferrozine: a new spectrophotometric reagent for iron. Analytical Chemistry 42(7): 779–781. 10.1021/ac60289a016

[33] Su Q, Bazylinski D A, Jensen M M. (2023). Effect of oxic and anoxic conditions on intracellular storage of polyhydroxyalkanoate and polyphosphate in Magnetospirillum magneticum strain AMB-1. Frontiers in Microbiology, 14: 1203805

[34] Sun W, Lin Z, Yu Q, Cheng S, Gao H. (2021). Promoting extracellular electron transfer of Shewanella oneidensis MR-1 by optimizing the periplasmic cytochrome c network. Frontiers in Microbiology, 12: 727709

[35] Sund C J, McMasters S, Crittenden S R, Harrell L E, Sumner J J. (2007). Effect of electron mediators on current generation and fermentation in a microbial fuel cell. Applied Microbiology and Biotechnology, 76(3): 561–568

[36] Uebe R, Schüler D. (2016). Magnetosome biogenesis in magnetotactic bacteria. Nature Reviews. Microbiology, 14(10): 621–637

[37] Voordeckers J W, Kim B C, Izallalen M, Lovley D R. (2010). Role of Geobacter sulfurreducens outer surface c-type cytochromes in reduction of soil humic acid and anthraquinone-2,6-disulfonate. Applied and Environmental Microbiology, 76(7): 2371–2375

[38] Wang H, Ren Z J. (2013). A comprehensive review of microbial electrochemical systems as a platform technology. Biotechnology Advances, 31(8): 1796–1807

[39] Wang X, Li Y, Zhao J, Yao H, Chu S, Song Z, He Z, Zhang W. (2020). Magnetotactic bacteria: characteristics and environmental applications. Frontiers of Environmental Science & Engineering, 14(4): 56

[40] Wessel A K, Arshad T A, Fitzpatrick M, Connell J L, Bonnecaze R T, Shear J B, Whiteley M. (2014). Oxygen limitation within a bacterial aggregate. mBio, 5(2): e00992–14

[41] Yalcin S E, O’Brien J P, Gu Y, Reiss K, Yi S M, Jain R, Srikanth V, Dahl P J, Huynh W, Vu D, Acharya A, Chaudhuri S, Varga T, Batista V S, Malvankar N S. (2020). Electric field stimulates production of highly conductive microbial OmcZ nanowires. Nature Chemical Biology, 16(10): 1136–1142

[42] Yamasaki R, Maeda T, Wood T K. (2018). Electron carriers increase electricity production in methane microbial fuel cells that reverse methanogenesis. Biotechnology for Biofuels, 11(1): 211

[43] YeeM OJoerg DAlfredSRotaruA E (2020). Cultivating electroactive microbes: from field to bench. Nanotechnology, 31(17), 174003

[44] Yu N Y, Laird M R, Spencer C, Brinkman F S L. (2011). PSORTdb: an expanded, auto-updated, user-friendly protein subcellular localization database for Bacteria and Archaea. Nucleic Acids Research, 39(Database): D241–D244

[45] Zou L, Zhu F, Long Z, Huang Y. (2021). Bacterial extracellular electron transfer: a powerful route to the green biosynthesis of inorganic nanomaterials for multifunctional applications. Journal of Nanobiotechnology, 19(1): 120

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The Author(s) 2024. This article is published with open access at link.springer.com and journal.hep.com.cn