Electroactivity of the magnetotactic bacteria <i>Magnetospirillum magneticum</i> AMB-1 and <i>Magnetospirillum gryphiswaldense</i> MSR-1

doi:10.1007/s11783-024-1808-3

Front. Environ. Sci. Eng.

2024, Vol. 18

Issue (4) : 48 https://doi.org/10.1007/s11783-024-1808-3

RESEARCH ARTICLE

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

Mathias Fessler, Qingxian Su, Marlene Mark Jensen(

), Yifeng Zhang(

)

Department of Environmental and Resource Engineering, Technical University of Denmark, Copenhagen, DK-2800, Denmark

Download: PDF(1621 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

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.

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

Corresponding Author(s): Marlene Mark Jensen,Yifeng Zhang

Issue Date: 21 December 2023

Cite this article:

Mathias Fessler,Qingxian Su,Marlene Mark Jensen, et al. Electroactivity of the magnetotactic bacteria Magnetospirillum magneticum AMB-1 and Magnetospirillum gryphiswaldense MSR-1[J]. Front. Environ. Sci. Eng., 2024, 18(4): 48.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-024-1808-3
https://academic.hep.com.cn/fese/EN/Y2024/V18/I4/48

Fig.1 Power density of M. magneticum and M. gryphiswaldense in MFCs (A, n = 2), and growth in serum bottles with NaNO₃ and 1% O₂ (B, n = 4). Error bars show standard deviation.

Fig.2 Reduction of Fe₂O₃ (A, n = 3) and FeOOH (B, n = 3) by M. magneticum and M. gryphiswaldense. Error bars show standard deviation and the controls are uninoculated medium.

Fig.3 Fe₂O₃ reduction by M. magneticum and M. gryphiswaldense in cultures with resazurin (A, n = 3), humic acid (B, n = 3), neutral red (C, n = 3), and AQDS (D, n = 3). Error bars show standard deviation and the controls are uninoculated medium.

1	M Amor, F P Mathon, C L Monteil, V Busigny, C T Lefevre. (2020). Iron-biomineralizing organelle in magnetotactic bacteria: function, synthesis and preservation in ancient rock samples. Environmental Microbiology, 22(9): 3611–3632 https://doi.org/10.1111/1462-2920.15098
2	D Coursolle, D B Baron, D R Bond, J A Gralnick. (2010). The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis. Journal of Bacteriology, 192(2): 467–474 https://doi.org/10.1128/JB.00925-09
3	R Fathey, O M Gomaa, A E H Ali, H A El Kareem, M A Zaid. (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 https://doi.org/10.1007/s13213-015-1152-8
4	E Y Fernando, T Keshavarz, G Kyazze. (2019). The use of bioelectrochemical systems in environmental remediation of xenobiotics: a review. Journal of Chemical Technology and Biotechnology, 94(7): 2070–2080 https://doi.org/10.1002/jctb.5848
5	M Fessler, J S Madsen, Y Zhang. (2022). Microbial interactions in electroactive biofilms for environmental engineering applications: a role for nonexoelectrogens. Environmental Science & Technology, 56(22): 15273–15279 https://doi.org/10.1021/acs.est.2c04368
6	M Fessler, J S Madsen, Y Zhang. (2023). Conjugative plasmids inhibit extracellular electron transfer in Geobacter sulfurreducens. Frontiers in Microbiology, 14: 1150091 https://doi.org/10.3389/fmicb.2023.1150091
7	D J Filman, S F Marino, J E Ward, L Yang, Z Mester, E Bullitt, D R Lovley, M Strauss. (2019). Cryo-EM reveals the structural basis of long-range electron transport in a cytochrome-based bacterial nanowire. Communications Biology, 2(1): 219 https://doi.org/10.1038/s42003-019-0448-9
8	N R Glasser, S H Saunders, D K Newman. (2017). The colorful world of extracellular electron shuttles. Annual Review of Microbiology, 71(1): 731–751 https://doi.org/10.1146/annurev-micro-090816-093913
9	Y Gu, V Srikanth, A I Salazar-Morales, R Jain, J P O’Brien, S M Yi, R K Soni, F A Samatey, S E Yalcin, N S Malvankar. (2021). Structure of Geobacter pili reveals secretory rather than nanowire behaviour. Nature, 597(7876): 430–434 https://doi.org/10.1038/s41586-021-03857-w
10	A Hirose, T Kasai, M Aoki, T Umemura, K Watanabe, A Kouzuma. (2018). Electrochemically active bacteria sense electrode potentials for regulating catabolic pathways. Nature Communications, 9(1): 1083 https://doi.org/10.1038/s41467-018-03416-4
11	D E Holmes, Y Dang, D J F Walker, D R Lovley. (2016). The electrically conductive pili of Geobacter species are a recently evolved feature for extracellular electron transfer. Microbial Genomics, 2(8): e000072 https://doi.org/10.1099/mgen.0.000072
12	Z Jiang, Q Liu, M J Dekkers, V Barron, J Torrent, A P Roberts. (2016). Control of Earth-like magnetic fields on the transformation of ferrihydrite to hematite and goethite. Scientific Reports, 6(1): 30395 https://doi.org/10.1038/srep30395
13	C Koch, F Harnisch (2016). Is there a specific ecological niche for electroactive microorganisms? ChemElectroChem, 3(9): 1282–1295 10.1002/celc.201600079
14	V Lanas, B E Logan. (2013). Evaluation of multi-brush anode systems in microbial fuel cells. Bioresource Technology, 148: 379–385 https://doi.org/10.1016/j.biortech.2013.08.154
15	L Le Nagard, V Morillo-López, C Fradin, D A Bazylinski (2018). Growing magnetotactic bacteria of the genus magnetospirillum: strains MSR-1, AMB-1 and MS-1. Journal of Visualized Experiments: JoVE
16	C T Lefèvre, M Bennet, L Landau, P Vach, D Pignol, D A Bazylinski, R B Frankel, S Klumpp, D Faivre. (2014). Diversity of magneto-aerotactic behaviors and oxygen sensing mechanisms in cultured magnetotactic bacteria. Biophysical Journal, 107(2): 527–538 https://doi.org/10.1016/j.bpj.2014.05.043
17	C E Levar, C L Hoffman, A J Dunshee, B M Toner, D R Bond (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	M Li, X L Yu, Y W Li, W Han, P F Yu, K Lun Yeung, C H Mo, S Q Zhou. (2022). Investigating the electron shuttling characteristics of resazurin in enhancing bio-electricity generation in microbial fuel cell. Chemical Engineering Journal, 428: 130924 https://doi.org/10.1016/j.cej.2021.130924
19	S L Li,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	W Lin, W Zhang, X Zhao, A P Roberts, G A Paterson, D A Bazylinski, Y Pan. (2018). Genomic expansion of magnetotactic bacteria reveals an early common origin of magnetotaxis with lineage-specific evolution. ISME Journal, 12(6): 1508–1519 https://doi.org/10.1038/s41396-018-0098-9
21	B E Logan, R Rossi, A Ragab, P E Saikaly. (2019). Electroactive microorganisms in bioelectrochemical systems. Nature Reviews. Microbiology, 17(5): 307–319 https://doi.org/10.1038/s41579-019-0173-x
22	D R Lovley, E J Phillips. (1986). Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Applied and Environmental Microbiology, 51(4): 683–689 https://doi.org/10.1128/aem.51.4.683-689.1986
23	D R Lovley, D J F Walker. (2019). Geobacter protein nanowires. Frontiers in Microbiology, 10: 2078 https://doi.org/10.3389/fmicb.2019.02078
24	E Marsili, D B Baron, I D Shikhare, D Coursolle, J A Gralnick, D R Bond. (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 https://doi.org/10.1073/pnas.0710525105
25	T Matsunaga, Y Okamura, Y Fukuda, A T Wahyudi, Y Murase, H Takeyama. (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 https://doi.org/10.1093/dnares/dsi002
26	T Matsunaga, T Sakaguchi, F Tadakoro. (1991). Magnetite formation by a magnetic bacterium capable of growing aerobically. Applied Microbiology and Biotechnology, 35(5): 651–655 https://doi.org/10.1007/BF00169632
27	C Moisescu, I Ardelean, L Benning. (2014). The effect and role of environmental conditions on magnetosome synthesis. Frontiers in Microbiology, 5(49): 1–12 https://doi.org/10.3389/fmicb.2014.00049
28	G Reguera, K D McCarthy, T Mehta, J S Nicoll, M T Tuominen, D R Lovley. (2005). Extracellular electron transfer via microbial nanowires. Nature, 435(7045): 1098–1101 https://doi.org/10.1038/nature03661
29	D Schüler, M Köhler. (1992). The isolation of a new magnetic spirillum. Zentralblatt für Mikrobiologie, 147(1–2): 150–151 https://doi.org/10.1016/S0232-4393(11)80377-X
30	B A Smit, Zyl E Van, J J Joubert, W Meyer, S Prévéral, C T Lefèvre, S N Venter. (2018). Magnetotactic bacteria used to generate electricity based on Faraday’s law of electromagnetic induction. Letters in Applied Microbiology, 66(5): 362–367 https://doi.org/10.1111/lam.12862
31	K L Straub, M Benz, B Schink. (2001). Iron metabolism in anoxic environments at near neutral pH. FEMS Microbiology Ecology, 34(3): 181–186 https://doi.org/10.1111/j.1574-6941.2001.tb00768.x
32	L L Stookey (1970). Ferrozine: a new spectrophotometric reagent for iron. Analytical Chemistry 42(7): 779–781. 10.1021/ac60289a016
33	Q Su, D A Bazylinski, M M Jensen. (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 https://doi.org/10.3389/fmicb.2023.1203805
34	W Sun, Z Lin, Q Yu, S Cheng, H Gao. (2021). Promoting extracellular electron transfer of Shewanella oneidensis MR-1 by optimizing the periplasmic cytochrome c network. Frontiers in Microbiology, 12: 727709 https://doi.org/10.3389/fmicb.2021.727709
35	C J Sund, S McMasters, S R Crittenden, L E Harrell, J J Sumner. (2007). Effect of electron mediators on current generation and fermentation in a microbial fuel cell. Applied Microbiology and Biotechnology, 76(3): 561–568 https://doi.org/10.1007/s00253-007-1038-1
36	R Uebe, D Schüler. (2016). Magnetosome biogenesis in magnetotactic bacteria. Nature Reviews. Microbiology, 14(10): 621–637 https://doi.org/10.1038/nrmicro.2016.99
37	J W Voordeckers, B C Kim, M Izallalen, D R Lovley. (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 https://doi.org/10.1128/AEM.02250-09
38	H Wang, Z J Ren. (2013). A comprehensive review of microbial electrochemical systems as a platform technology. Biotechnology Advances, 31(8): 1796–1807 https://doi.org/10.1016/j.biotechadv.2013.10.001
39	X Wang, Y Li, J Zhao, H Yao, S Chu, Z Song, Z He, W Zhang. (2020). Magnetotactic bacteria: characteristics and environmental applications. Frontiers of Environmental Science & Engineering, 14(4): 56 https://doi.org/10.1007/s11783-020-1235-z
40	A K Wessel, T A Arshad, M Fitzpatrick, J L Connell, R T Bonnecaze, J B Shear, M Whiteley. (2014). Oxygen limitation within a bacterial aggregate. mBio, 5(2): e00992–14 https://doi.org/10.1128/mBio.00992-14
41	S E Yalcin, J P O’Brien, Y Gu, K Reiss, S M Yi, R Jain, V Srikanth, P J Dahl, W Huynh, D Vu, A Acharya, S Chaudhuri, T Varga, V S Batista, N S Malvankar. (2020). Electric field stimulates production of highly conductive microbial OmcZ nanowires. Nature Chemical Biology, 16(10): 1136–1142 https://doi.org/10.1038/s41589-020-0623-9
42	R Yamasaki, T Maeda, T K Wood. (2018). Electron carriers increase electricity production in methane microbial fuel cells that reverse methanogenesis. Biotechnology for Biofuels, 11(1): 211 https://doi.org/10.1186/s13068-018-1208-7
43	M O YeeD JoergS AlfredA E (2020) Rotaru. Cultivating electroactive microbes: from field to bench. Nanotechnology, 31(17), 174003
44	N Y Yu, M R Laird, C Spencer, F S L Brinkman. (2011). PSORTdb: an expanded, auto-updated, user-friendly protein subcellular localization database for Bacteria and Archaea. Nucleic Acids Research, 39(Database): D241–D244 https://doi.org/10.1093/nar/gkq1093
45	L Zou, F Zhu, Z Long, Y Huang. (2021). Bacterial extracellular electron transfer: a powerful route to the green biosynthesis of inorganic nanomaterials for multifunctional applications. Journal of Nanobiotechnology, 19(1): 120 https://doi.org/10.1186/s12951-021-00868-7

[1]	Yingbin Hu, Ning Li, Jin Jiang, Yanbin Xu, Xiaonan Luo, Jie Cao. Simultaneous Feammox and anammox process facilitated by activated carbon as an electron shuttle for autotrophic biological nitrogen removal[J]. Front. Environ. Sci. Eng., 2022, 16(7): 90-.
[2]	Yuqing Yan, Xin Wang. Integrated energy view of wastewater treatment: A potential of electrochemical biodegradation[J]. Front. Environ. Sci. Eng., 2022, 16(4): 52-.
[3]	Xinjie Wang, Yang Li, Jian Zhao, Hong Yao, Siqi Chu, Zimu Song, Zongxian He, Wen Zhang. Magnetotactic bacteria: Characteristics and environmental applications[J]. Front. Environ. Sci. Eng., 2020, 14(4): 56-.
[4]	Xingguo Guo, Qiuying Wang, Ting Xu, Kajia Wei, Mengxi Yin, Peng Liang, Xia Huang, Xiaoyuan Zhang. One-step ball milling-prepared nano Fe₂O₃ and nitrogen-doped graphene with high oxygen reduction activity and its application in microbial fuel cells[J]. Front. Environ. Sci. Eng., 2020, 14(2): 30-.
[5]	Feng ZHANG,Shengsong YU,Jie LI,Wenwei LI,Hanqing YU. *Mechanisms behind the accelerated extracellular electron transfer in Geobacter sulfurreducens* DL-1 by modifying gold electrode with self-assembled monolayers**[J]. Front. Environ. Sci. Eng., 2016, 10(3): 531-538.
[6]	Yong XIAO,Yue ZHENG,Song WU,Zhao-Hui YANG,Feng ZHAO. Nitrogen recovery from wastewater using microbial fuel cells[J]. Front. Environ. Sci. Eng., 2016, 10(1): 185-191.

Viewed

Full text

Abstract

Cited

Shared

Discussed