Redox control of magnetosome biomineralization

Yingjie LI

doi:10.1007/s00343-021-0422-5

Your Location：

Home >

Browse articles >

Redox control of magnetosome biomineralization

Special Section: Magnetotactic Bacteria and Magnetoreception | Updated：2023-05-20

- Redox control of magnetosome biomineralization
- Journal of Oceanology and Limnology Vol. 39, Issue 6, Pages: 2070-2081(2021)
- Affiliations：
  
  State Key Laboratory of Microbial Technology, Shandong University, Qingdao 266237, China
- Author bio：
  
  Yingjie LI, yingjie.li@sdu.edu.cn
- Funds：
- DOI：10.1007/s00343-021-0422-5
  CLC：
- Received：03 November 2020，
  
  Accepted：15 December 2020，
  
  Online First：27 December 2020，
  
  Published：2021-11
- Accepted：
Scan QR Code
Yingjie LI. Redox control of magnetosome biomineralization[J]. Journal of Oceanology and Limnology, 2021, 39(6): 2070-2081.
DOI：

Yingjie LI. Redox control of magnetosome biomineralization[J]. Journal of Oceanology and Limnology, 2021, 39(6): 2070-2081. DOI： 10.1007/s00343-021-0422-5.

摘要

Abstract

Magnetotactic bacteria can orientate in the Earth's magnetic field to search for their preferred microoxic environments

which is achieved by their unique organelles

the magnetosomes. Magnetosomes contain nanometer-sized crystal particles of magnetic iron minerals

which are only synthesized in lowoxygen environments. Although the mechanism of aerobic repression for magnetosome biomineralization has not yet fully understood

a series of studies have verified that redox modulation is pivotal for magnetosome formation. In this review

these advances in redox modulation for magnetosome biosynthesis are highlighted

mainly including respiration pathway enzymes

specific magnetosome-associated redox proteins

and oxygen- or nitrate-sensing regulators. Furthermore

their relationship during magnetosome biomineralization is discussed to give insight into redox control and biomineralization and inspire potential solutions for the application of respiration pathways to improve the yields of magnetosome.

关键词

Keywords

references

Adamczack J, Hoffmann M, Papke U, Haufschildt K, Nicke T, Bröring M, Sezer M, Weimar R, Kuhlmann U, Hildebrandt P, Layer G. 2014. NirN protein from Pseudomonas aeruginosa is a novel electron-bifurcating dehydrogenase catalyzing the last step of heme d 1 biosynthesis. The Journal of Biological Chemistry , 289 (44): 30753-30762, https://doi.org/10.1074/jbc.M114.603886..

Bazylinski D A, Blakemore R P. 1983. Denitrification and assimilatory nitrate reduction in Aquaspirillum magnetotacticum . Applied and Environmental Microbiology , 46 (5): 1118-1124, https://doi.org/10.1128/AEM.46.5.1118-1124.1983..

Bazylinski D A, Williams T J. 2006. Ecophysiology of magnetotactic bacteria. In : Schüler D ed. Magnetoreception and Magnetosomes in Bacteria. Springer, Heidelberg. p. 37-75, https://doi.org/10.1007/7171_038.

Blakemore R P, Short K A, Bazylinski D A, Rosenblatt C, Frankel R B. 1985. Microaerobic conditions are required for magnetite formation within Aquaspirillum magnetotacticum . Geomicrobiology Journal , 4 (1): 53-71, https://doi.org/10.1080/01490458509385920..

Bueno E, Mesa S, Bedmar E J, Richardson D J, Delgado M J. 2012. Bacterial adaptation of respiration from oxic to microoxic and anoxic conditions: redox control. Antioxidants & Redox Signaling , 16 (8): 819-852, https://doi.org/10.1089/ars.2011.4051..

Chandrangsu P, Rensing C, Helmann J D. 2017. Metal homeostasis and resistance in bacteria. Nature Reviews Microbiology , 15 (6): 338-350, https://doi.org/10.1038/nrmicro.2017.15..

Faivre D, Agrinier P, Menguy N, Zuddas P, Pachana K, Gloter A, Laval J Y, Guyot F. 2004. Mineralogical and isotopic properties of inorganic nanocrystalline magnetites. Geochimica et Cosmochimica Acta , 68 (21): 4395-4403, https://doi.org/10.1016/j.gca.2004.03.016..

Faivre D, Böttger L H, Matzanke B F, Schüler D. 2007. Intracellular magnetite biomineralization in bacteria proceeds by a distinct pathway involving membrane-bound ferritin and an iron(II) species. Angewandte Chemie International Edition , 46 (44): 8495-8499, https://doi.org/10.1002/anie.200700927..

Faivre D, Schüler D. 2008. Magnetotactic bacteria and magnetosomes. Chemical Reviews , 108 (11): 4875-4898, https://doi.org/10.1021/cr078258w..

Grünberg K, Müller E C, Otto A, Reszka R, Linder D, Kube M, Reinhardt R, Schüler D. 2004. Biochemical and proteomic analysis of the magnetosome membrane in Magnetospirillum gryphiswaldense . Applied and Environmental Microbiology , 70 (2): 1040-1050, https://doi.org/10.1128/aem.70.2.1040-1050.2004..

Hamada M, Toyofuku M, Miyano T, Nomura N. 2014. cbb 3 -type cytochrome c oxidases, aerobic respiratory enzymes, impact the anaerobic life of Pseudomonas aeruginosa PAO1. Journal of Bacteriology , 196 (22): 3881-3889, https://doi.org/10.1128/JB.01978-14..

Jogler C, Schüler D. 2009. Genomics, genetics, and cell biology of magnetosome formation. Annual Review of Microbiology , 63 : 501-521, https://doi.org/10.1146/annurev.micro.62.081307.162908..

Jones S R, Wilson T D, Brown M E, Rahn-Lee L, Yu Y, Fredriksen L L, Ozyamak E, Komeili A, Chang M C Y. 2015. Genetic and biochemical investigations of the role of MamP in redox control of iron biomineralization in Magnetospirillum magneticum . Pro c eedings of the National Academy of S ci ences of the United States of America , 112 (13): 3904-3909, https://doi.org/10.1073/pnas.1417614112..

Klünemann T, Preuß A, Adamczack J, Rosa L F M, Harnisch F, Layer G, Blankenfeldt W. 2019. Crystal structure of dihydro-heme d 1 dehydrogenase NirN from Pseudomonas aeruginosa reveals amino acid residues essential forcatalysis. Journal of Molecular Biology , 431 (17): 3246-3260, https://doi.org/10.1016/j.jmb.2019.05.046..

Kolinko I, Lohße A, Borg S, Raschdorf O, Jogler C, Tu Q, Pósfai M, Tompa É, Plitzko J M, Brachmann A, Wanner G, Müller R, Zhang Y M, Schüler D. 2014. Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters. Nature Nanotechnology , 9 (3): 193-197, https://doi.org/10.1038/nnano.2014.13..

Li Y J, Bali S, Borg S, Schüler D. 2013. Cytochrome cd 1 nitrite reductase NirS is involved in anaerobic magnetite biomineralization in Magnetospirillum gryphiswaldense and requires NirN for proper d 1 heme assembly. Journal of Bacteriology , 195 (18): 4297-4309, https://doi.org/10.1128/JB.00686-13..

Li Y J, Katzmann E, Borg S, Schüler D. 2012. The periplasmic nitrate reductase Nap is required for anaerobic growth and involved in redox control of magnetite biomineralization in Magnetospirillum gryphiswaldense . Journal of Bacteriology , 194 (18): 4847-4856, https://doi.org/10.1128/JB.00903-12..

Li Y J, Raschdorf O, Silva K T, Schüler D. 2014a. The terminal oxidase cbb 3 functions in redox control of magnetite biomineralization in Magnetospirillum gryphiswaldense . Journal of Bacteriology , 196 (14): 2552-2562, https://doi.org/10.1128/JB.01652-14..

Li Y J, Sabaty M, Borg S, Silva K T, Pignol D, Schüler D. 2014b. The oxygen sensor MgFnr controls magnetite biomineralization by regulation of denitrification in Magnetospirillum gryphiswaldense . BMC Microbiology , 14 : 153, https://doi.org/10.1186/1471-2180-14-153..

Lohße A, Borg S, Raschdorf O, Kolinko I, Tompa É, Pósfai M, Faivre D, Baumgartner J, Schüler D. 2014. Genetic dissection of the mamAB and mms6 operons reveals a gene set essential for magnetosome biogenesis in Magnetospirillum gryphiswaldense . Journal of Bacteriology , 196 (14): 2658-2669, https://doi.org/10.1128/JB.01716-14..

Lohße A, Kolinko I, Raschdorf O, Uebe R, Borg S, Brachmann A, Plitzko J M, Müller R, Zhang Y M, Schüler D, Vieille C. 2016. Overproduction of magnetosomes by genomic amplification of biosynthesis-related gene clusters in a magnetotactic bacterium. Applied and Environmental Microbiology , 82 (10): 3032-3041, https://doi.org/10.1128/AEM.03860-15..

Lohße A, Ullrich S, Katzmann E, Borg S, Wanner G, Richter M, Voigt B, Schweder T, Schüler D. 2011. Functional analysis of the magnetosome island in Magnetospirillum gryphiswaldense : the mamAB operon is suﬃcient formagnetite biomineralization. PLoS One , 6 (10): e25561, https://doi.org/10.1371/journal.pone.0025561..

Lower B H, Bazylinski D A. 2013. The bacterial magnetosome: a unique prokaryotic organelle. Journal of Molecular Microbiology and Biotechnology , 23 (1-2): 63-80, https://doi.org/10.1159/000346543..

Mandernack K W, Bazylinski D A, Shanks III W C, Bullen T W. 1999. Oxygen and iron isotope studies of magnetite produced by magnetotactic bacteria. Science , 285 (5435): 1892-1896, https://doi.org/10.1126/science.285.5435.1892..

Mann S, Sparks N H C, Board R G. 1990. Magnetotactic bacteria: microbiology, biomineralization, palaeomagnetism and biotechnology. Advances in Microbial Physiology , 31 : 125-181, https://doi.org/10.1016/S0065-2911(08)60121-6..

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, https://doi.org/10.1007/BF00169632..

Matsunaga T, Tsujimura N. 1993. Respiratory inhibitors of a magnetic bacterium Magnetospirillum sp. AMB-1 capable of growing aerobically. Applied Microbiology and Biotechnology , 39 (3): 368-371, https://doi.org/10.1007/BF00192094..

Mayfield J A, Dehner C A, DuBois J L. 2011. Recent advances in bacterial heme protein biochemistry. Current Opinion in Chemical Biology , 15 (2): 260-266, https://doi.org/10.1016/j.cbpa.2011.02.002..

McCausland H C, Komeili A. 2020. Magnetic genes: studying the genetics of biomineralization in magnetotactic bacteria. PLoS Genetics , 16 (2): e1008499, https://doi.org/10.1371/journal.pgen.1008499..

Müller F D, Raschdorf O, Nudelman H, Messerer M, Katzmann E, Plitzko J M, Zarivach R, Schüler D. 2014. The FtsZ-Like protein FtsZm of Magnetospirillum gryphiswaldense likely interacts with its generic homolog and is required for biomineralization under nitrate deprivation. Journal of Bacteriology , 196 (3): 650-659, https://doi.org/10.1128/JB.00804-13..

Murat D, Quinlan A, Vali H, Komeili A. 2010. Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle. Proceedings of the National Academy of Sciences of the United States of America , 107 (12): 5593-5598, https://doi.org/10.1073/pnas.0914439107..

Nicke T, Schnitzer T, Münch K, Adamczack J, Haufschildt K, Buchmeier S, Kucklick M, Felgenträger U, Jänsch L, Riedel K, Layer G. 2013. Maturation of the cytochrome cd 1 nitrite reductase NirS from Pseudomonas aeruginosa requires transient interactions between the three proteins NirS, NirN and NirF. Bioscience Reports , 33 (3): e00048, https://doi.org/10.1042/BSR20130043..

O'Brien W, Paoletti L C, Blakemore R P. 1987. Spectral analysis of cytochromes in Aquaspirillum magnetotacticum . Current Microbiology , 15 (3): 121-127, https://doi.org/10.1007/BF01577258..

Qi L, Li J, Zhang W J, Liu J N, Rong C B, Li Y, Wu L F. 2012. Fur in Magnetospirillum gryphiswaldense influences magnetosomes formation and directly regulates the genes involved in iron and oxygen metabolism. PLoS One , 7 (1): e29572, https://doi.org/10.1371/journal.pone.0029572..

Quinlan A, Murat D, Vali H, Komeili A. 2011. The HtrA/DegP family protease MamE is a bifunctional protein with roles in magnetosome protein localization and magnetite biomineralization. Molecular Microbiology , 80 (4): 1075-1087, https://doi.org/10.1111/j.1365-2958.2011.07631.x..

Rahn-Lee L, Komeili A. 2013. The magnetosome model: insights into the mechanisms of bacterial biomineralization. Frontiers in Microbiology , 4 : 352, https://doi.org/10.3389/fmicb.2013.00352..

Raschdorf O, Forstner Y, Kolinko I, Uebe R, Plitzko J M, Schüler D. 2016. Genetic and ultrastructural analysis reveals the key players and initial steps of bacterial magnetosome membrane biogenesis. PLoS Genetics , 12 (6): e1006101, https://doi.org/10.1371/journal.pgen.1006101..

Raschdorf O, Müller F D, Pósfai M, Plitzko J M, Schüler D.2013. The magnetosome proteins MamX, MamZ and MamH are involved in redox control of magnetite biomineralization in Magnetospirillum gryphiswaldense . Molecular Microbiology , 89 (5): 872-886, https://doi.org/10.1111/mmi.12317..

Sakaguchi H, Hagiwara H, Fukumori Y, Tamaura Y, Funaki M, Hirose S. 1993. Oxygen concentration-dependent induction of a 140-kDa protein in magnetic bacterium Magnetospirillum magnetotacticum MS-1. FEMS Microbiology Letters , 107 (2-3): 169-173, https://doi.org/10.1111/j.1574-6968.1993.tb06025.x..

Schübbe S, Wurdemann C, Peplies J, Heyen U, Wawer C, Glöckner F O, Schüler D. 2006. Transcriptional organization and regulation of magnetosome operons in Magnetospirillum gryphiswaldense . Applied and Environmental Microbiology , 72 (9): 5757-5765, https://doi.org/10.1128/AEM.00201-06..

Schüler D. 2008. Genetics and cell biology of magnetosome formation in magnetotactic bacteria. FEMS Microbiology Reviews , 32 (4): 654-672, https://doi.org/10.1111/j.1574-6976.2008.00116.x..

Short K A, Blakemore R P. 1989. Periplasmic superoxide dismutases in Aquaspirillum magnetotacticum . Archives of Microbiology , 152 (4): 342-346, https://doi.org/10.1007/BF00425171..

Siponen M I, Adryanczyk G, Ginet N, Arnoux P, Pignol D. 2012. Magnetochrome: a c -type cytochrome domain specific to magnetotatic bacteria. Biochemical Society Transactions , 40 (6): 1319-1323, https://doi.org/10.1042/BST20120104..

Siponen M I, Legrand P, Widdrat M, Jones S R, Zhang W J, Chang M C Y, Faivre D, Arnoux P, Pignol D. 2013. Structural insight into magnetochrome-mediated magnetite biomineralization. Nature , 502 (7473): 681-684, https://doi.org/10.1038/nature12573..

Tamegai H, Fukumori Y. 1994. Purification, and some molecular and enzymatic features of a novel ccb -type cytochrome c oxidase from a microaerobic denitrifier, Magnetospirillum magnetotacticum . FEBS Letters , 347 (1): 22-26, https://doi.org/10.1016/0014-5793(94)00500-1..

Tamegai H, Yamanaka T, Fukumori Y. 1993. Purification and properties of a 'cytochrome a 1 '-like hemoprotein from a magnetotactic bacterium, Aquaspirillum magnetotacticum . Biochimica et Biophysica Acta ( BBA )- General Subjects , 1158 (3): 237-243, https://doi.org/10.1016/0304-4165(93)90020-9..

Toro-Nahuelpan M, Giacomelli G, Raschdorf O, Borg S, Plitzko J M, Bramkamp M, Schüler D, Müller F D. 2019. MamY is a membrane-bound protein that aligns magnetosomes and the motility axis of helical magnetotactic bacteria. Nature Microbiology , 4 (11): 1978-1989, https://doi.org/10.1038/s41564-019-0512-8..

Torres M J, Avila S, Bedmar E J, Delgado M J. 2018. Overexpression of the periplasmic nitrate reductase supports anaerobic growth by Ensifer meliloti . FEMS Microbiology Letters , 365 (7): fny041, https://doi.org/10.1093/femsle/fny041..

Uebe R, Schüler D. 2016. Magnetosome biogenesis in magnetotactic bacteria. Nature Reviews Microbiology , 14 (10): 621-637, https://doi.org/10.1038/nrmicro.2016.99..

Uebe R, Voigt B, Schweder T, Albrecht D, Katzmann E, Lang C, Böttger L, Matzanke B, Schüler D. 2010. Deletion of a fur- like gene affects iron homeostasis and magnetosome formation in Magnetospirillum gryphiswaldense . Journal of Bacteriology , 192 (16): 4192-4204, https://doi.org/10.1128/JB.00319-10..

Ullrich S, Kube M, Schübbe S, Reinhardt R, Schüler D. 2005. A hypervariable 130-kilobase genomic region of Magnetospirillum gryphiswaldense comprises amagnetosome island which undergoes frequent rearrangements during stationary growth. Journal of Bacteriology , 187 (21): 7176-7184, https://doi.org/10.1128/JB.187.21.7176-7184.2005..

Unden G, Becker S, Bongaerts J, Holighaus G, Schirawski J, Six S. 1995. O 2 -sensing and O 2 -dependent gene regulation in facultatively anaerobic bacteria. Archives of Microbiology , 164 (2): 81-90, https://doi.org/10.1007/BF02525312..

Wang K, Ge X, Bo T, Chen Q, Chen G, Liu W. 2011. Interruption of the denitrification pathway influences cell growth and magnetosome formation in Magnetospirillum magneticum AMB-1. Letters in Applied Microbiology , 53 (1): 55-62, https://doi.org/10.1111/j.1472-765X.2011.03063.x..

Wang Q, Wang M W, Wang X, Guan G H, Li Y, Peng Y L, Li J L. 2015. Iron response regulator protein IrrB in Magnetospirillum gryphiswaldense MSR-1 helps controlthe iron/oxygen balance, oxidative stress tolerance, and magnetosome formation. Applied and Environmental Microbiology , 81 (23): 8044-8053, https://doi.org/10.1128/AEM.02585-15..

Wang Q, Wu S, Li X Y, Zhang T W, Yang J, Wang X, Li F, Li Y, Peng Y L, Li J L. 2019a. Work patterns of MamXY proteins during magnetosome formation in Magnetospirillum gryphiswaldense MSR-1. Applied and Environmental Microbiology , 85 (2): e02394-18, https://doi.org/10.1128/AEM.02394-18..

Wang X, Wang Q, Zhang Y, Wang Y J, Zhou Y, Zhang W J, Wen T, Li L, Zuo M Q, Zhang Z D, Tian J S, Jiang W, Li Y, Wang L, Li J L. 2016. Transcriptome analysis reveals physiological characteristics required for magnetosome formation in Magnetospirillum gryphiswaldense MSR-1. Environmental Microbiology Reports , 8 (3): 371-381, https://doi.org/10.1111/1758-2229.12395..

Wang X, Zheng H L, Wang Q, Jiang W, Wen Y, Tian J S, Sun J B, Li Y, Li J L. 2019b. Novel protein Mg2046 regulates magnetosome synthesis in Magnetospirillum gryphiswaldense MSR-1 by modulating a proper redoxstatus. Frontiers in Microbiology , 10 : 1478, https://doi.org/10.3389/fmicb.2019.01478..

Wen T, Guo F F, Zhang Y P, Tian J S, Li Y, Li J L, Jiang W. 2016. A novel role for Crp in controlling magnetosome biosynthesis in Magnetospirillum gryphiswaldense MSR-1. Scientific Reports , 6 : 21156, https://doi.org/10.1038/srep21156..

Yamazaki T, Oyanagi H, Fujiwara T, Fukumori Y. 1995. Nitrite reductase from the magnetotactic bacterium Magnetospirillum magnetotacticum . European Journal of Biochemistry , 233 (2): 665-671, https://doi.org/10.1111/j.1432-1033.1995.665_2.x..

Yang C D, Takeyama H, Tanaka T, Matsunaga T. 2001. Effects of growth medium composition, iron sources and atmospheric oxygen concentrations on production of luciferase-bacterial magnetic particle complex by a recombinant Magnetospirillum magneticum AMB-1. Enzyme and Microbial Technology , 29 (1): 13-19, https://doi.org/10.1016/S0141-0229(01)00343-X..

Yang J, Li S Q, Huang X L, Li J H, Li L, Pan Y X, Li Y. 2013. MamX encoded by the mamXY operon is involved in control of magnetosome maturation in Magnetospirillum gryphiswaldense MSR-1. BMC Microbiology , 13 : 203, https://doi.org/10.1186/1471-2180-13-203..

Zhang Y P, Wen T, Guo F F, Geng Y Y, Liu J Q, Peng T, Guan G H, Tian J S, Li Y, Li J L, Ju J, Jiang W. 2017. The disruption of an OxyR-Like protein impairs intracellular magnetite biomineralization in Magnetospirillum gryphiswaldense MSR-1. Frontiers in Microbiology , 8 : 208, https://doi.org/10.3389/fmicb.2017.00208..

Views

Downloads

CSCD

Alert me when the article has been cited

Submit

Tools

Publicity Resources

Observations on a magnetotactic bacteria-grazing ciliate in sediment from the intertidal zone of Huiquan Bay, China

Characterization and diversity of magnetotactic bacteria from sediments of Caroline Seamount in the Western Pacific Ocean

Morphological and phylogenetic diversity of magnetotactic bacteria and multicellular magnetotactic prokaryotes from a mangrove ecosystem in the Sanya River, South China

Magnetosymbiosis discovery: new perspectives in magnetotaxis research

Supplementation of alanine improves biomass accumulation and lipid production of Chlorella pyrenoidosa by increasing the respiratory and metabolic processes

Related Author

Si CHEN

Long-Fei WU

Wuchang ZHANG

Hongmiao PAN

Tian XIAO

Yicong ZHAO

Wenyan ZHANG

Kaixuan CUI

Related Institution

Aix Marseille Univ, CNRS, LCB, IM2 B, IMM

International Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms(LIA-MagMC), CNRS-CAS

Center for Ocean Mega-Science, Chinese Academy of Sciences

Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology (Qingdao)

University of Chinese Academy of Sciences

Address：Editorial Office of JOL, 88 Haijun Rd. Qingdao, 266000, China
Tel：+86-532-82898754 Email：jol@qdio.ac.cn
Technical support is provided by Beijing Founder electronics co., LTD 京ICP备09064830号-19 京公网安备11010802024621
It is recommended to read the content of this site in Chrome&IE9+. Please switch to extreme mode in browser 360.
Cookies We use cookies to help provide and enhance our service and tailor content. By continuing, you agree to the use of cookies.

⁰