Cite this paper:
Xinxin QIAN, Yicong ZHAO, Claire-Lise SANTINI, Hongmiao PAN, Tian XIAO, Haitao CHEN, Tao SONG, Jinhua LI, Francois ALBERTO, Sophie BRUSTLEIN, Long-Fei WU. How light affect the magnetotactic behavior and reproduction of ellipsoidal multicellular magnetoglobules?[J]. Journal of Oceanology and Limnology, 2021, 39(6): 2005-2014

How light affect the magnetotactic behavior and reproduction of ellipsoidal multicellular magnetoglobules?

Xinxin QIAN1,2, Yicong ZHAO3,4, Claire-Lise SANTINI2,3, Hongmiao PAN3,4, Tian XIAO3,4, Haitao CHEN3,5, Tao SONG3,5, Jinhua LI3,6, Francois ALBERTO2,3, Sophie BRUSTLEIN7, Long-Fei WU2,3
1 State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China;
2 Aix Marseille University, CNRS, LCB, Centuri, IM2 B, IMM, Marseille 13009, France;
3 International Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms(LIA-MagMC), CNRS-CAS, Marseille 13402, France;
4 CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
5 Institute of Electrical Engineering, Chinese Academy of Sciences, Beijing 100190, China;
6 Key Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing 100029, China;
7 Aix Marseille University, Centuri, Marseille 13009, France
Magnetotactic bacteria (MTB) synthesize intracellular magnetic organelles, magnetosomes, which consist of magnetic crystals that are enveloped in a membrane. Magnetosomes are organized into a chain(s) and confer on cells a magnetic dipolar moment. This magnetic property allows MTB cells to align and swim along geomagnetic field lines, a movement referred to as magnetotaxis. Some MTB species change their swim direction in response to illumination by UV, violet and blue light. Here we analyzed the polarity of morphology, magnetism, and motion in Mediterranean multicellular magnetotactic prokaryotes, also called, magnetoglobules or MMP. The magnetoglobules were assembled from 60–80 cells into an asymmetric ellipsoidal morphology with a relative narrow and large end. They swam dominantly northward, parallel to the direction of the magnetic field, with the narrow-end as the leading side. In response to a reversal in the direction of the magnetic field, they aligned quickly along the magnetic field lines and kept swimming northward. Interestingly, under constant illumination, 385-nm UV light, magnetoglobules changed their swimming direction southward anti-parallel to the direction of the magnetic field, with the large-end as the leading side. The change from a northward to southward direction occurred along with an increase of swimming speed. A minimum of 35-mW/cm2 irradiance of UV light was sufficient to trigger the swimming re-orientation. UV radiation also triggered the unidirectional division of magnetoglobules. Together these results revealed a coordination of the polarity of magnetoglobule morphology, magnetic moment, and swimming orientation, in response to magnetic and optical stimuli. The UV triggered the reversal of magnetotaxis and magnetoglobule division indicating the ecological significance of light for multicellular magnetotactic prokaryotes.
Key words:    photo-response|magnetic alignment|coordinated swimming   
Received: 2020-10-19   Revised: 2021-02-24
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Articles by Xinxin QIAN
Articles by Yicong ZHAO
Articles by Claire-Lise SANTINI
Articles by Hongmiao PAN
Articles by Tian XIAO
Articles by Haitao CHEN
Articles by Tao SONG
Articles by Jinhua LI
Articles by Francois ALBERTO
Articles by Sophie BRUSTLEIN
Articles by Long-Fei WU
Abreu F, Leão P, Vargas G, Cypriano J, Figueiredo V, EnrichPrast A, Bazylinski D A, Lins U. 2018. Culture-independent characterization of a novel magnetotactic member affiliated to the Beta class of the Proteobacteria phylum from an acidic lagoon. Environmental Microbiology, 20(7):2615-2624,
Abreu F, Morillo V, Nascimento F F, Werneck C, Cantão M E, Ciapina L P, De Almeida L G P, Lefèvre C T, Bazylinski D A, De Vasconcelos A T R, Lins U. 2013. Deciphering unusual uncultured magnetotactic multicellular prokaryotes through genomics. The ISME Journal, 8(5):1055-1068,
Bazylinski D A, Frankel R B. 2004. Magnetosome formation in prokaryotes. Nature Reviews Microbiology, 2(3):217-230,
Bazylinski D A, Lefèvre C T, Schüler D. 2013. Magnetotactic bacteria. In:Rosenberg E, DeLong E F, Lory S, Stackebrandt E, Thompson F eds. The Prokaryotes:Prokaryotic Physiology and Biochemistry. Springer, Berlin, Heidelberg. p.453-494.
Blakemore R P, Frankel R B, Kalmijn A J. 1980. South-seeking magnetotactic bacteria in the Southern Hemisphere. Nature, 286(5771):384-385,
Blakemore R. 1975. Magnetotactic bacteria. Science, 190(4212):377-379,
Chen C F, Ma Q F, Jiang W, Song T. 2011. Phototaxis in the magnetotactic bacterium Magnetospirillum magneticum strain AMB-1 is independent of magnetic fields. Applied Microbiology and Biotechnology, 90(1):269-275,
Chen H T, Li D D, Cai Y, Wu L F, Song T. 2020a. Bacteriophytochrome from Magnetospirillum magneticum affects phototactic behavior in response to light. FEMS Microbiology Letters, 367(17):fnaa142,
Chen H T, Li K F, Cai Y, Wang P P, Gong W M, Wu L F, Song T. 2020b. Light regulation of resistance to oxidative damage and magnetic crystal biogenesis in Magnetospirillum magneticum mediated by a Cys-less LOV-like protein. Applied Microbiology and Biotechnology, 104(18):7927-7941,
Chen Y R, Zhang R, Du H J, Pan H M, Zahng W Y, Zhou K, Li J H, Xiao T, Wu L F. 2015. A novel species of ellipsoidal multicellular magnetotactic prokaryotes from Lake Yuehu in China. Environmental Microbiology, 17(3):637-647,
Chen Y R, Zhang W Y, Zhou K, Pan H M, Du H J, Xu C, Xu J H, Pradel N, Santini C L, Li J H, Huang H, Pan Y X, Xiao T, Wu L F. 2016. Novel species and expanded distribution of ellipsoidal multicellular magnetotactic prokaryotes. Environmental Microbiology Report, 8(2):218-226,
De Azevedo L V, Acosta-Avalos D. 2015. Photokinesis is magnetic field dependent in the multicellular magnetotactic prokaryote Candidatus Magnetoglobus multicellularis. Antonie van Leeuwenhoek, 108(3):579-585,
De Azevedo L V, De Barros H L, Keim C N, Acosta-Avalos D. 2013. Effect of light wavelength on motility and magnetic sensibility of the magnetotactic multicellular prokaryote ‘Candidatus Magnetoglobus multicellularis’. Antonie van Leeuwenhoek, 104(3):405-412,
De Lins B H G, Esquivel D M, Farina M. 1990. Magnetotaxis. Science Progress, 74(295 Pt 3):347-359.
Frankel R B, Bazylinski D A, Johnson M S, Taylor B L. 1997. Magneto-aerotaxis in marine coccoid bacteria. Biophysical Journal, 73(2):994-1000,
Greenberg M, Canter K, Mahler I, Tornheim A. 2005. Observation of magnetoreceptive behavior in a multicellular magnetotactic prokaryote in higher than geomagnetic fields. Biophysical Journal, 88(2):1496-1499.
Keim C N, Abreu F, Lins U, De Barros H L, Farina M. 2004a. Cell organization and ultrastructure of a magnetotactic multicellular organism. Journal of Structural Biology, 145(3):254-262,
Keim C N, Martins J L, Abreu F, Rosado A S, De Barros H L, Borojevic R, Lins U, Farina M. 2004b. Multicellular life cycle of magnetotactic prokaryotes. FEMS Microbiology Letters, 240(2):203-208,
Li K F, Wang P P, Chen C F, Chen C Y, Li L L, Song T. 2017. Light irradiation helps magnetotactic bacteria eliminate intracellular reactive oxygen species. Environmental Microbiology, 19(9):3638-3648,
Lins U, Kachar B, Farina M. 1999. Imaging faces of shadowed magnetite (Fe3O4) crystals from magnetotactic bacteria with energy-filtering transmission electron microscopy. Microscopy Research & Technique, 46(4-5):319-324,<319::AID-JEMT9>3.0.CO;2-N.
Meijering E, Dzyubachyk O, Smal I. 2012. Chapter nineMethods for cell and particle tracking. Methods in Enzymology, 504:183-200,
Qian X X, Liu J, Menguy N, Li J H, Alberto F, Tang Z J, Xiao T, Zhang W Y, Wu L F. 2019. Identification of novel species of marine magnetotactic bacteria affiliated with Nitrospirae phylum. Environmental Microbiology Report, 11(3):330-337,
Qian X X, Santini C L, Kosta A, Menguy N, Guenno H L, Zhang W Y, Li J H, Chen Y R, Liu J, Alberto F, Espinosa L, Xiao T, Wu L F. 2020. Juxtaposed membranes underpin cellular adhesion and display unilateral cell division of multicellular magnetotactic prokaryotes. Environmental Microbiology, 22(4):1481-1494,
Rodgers F G, Blakemore R P, Blakemore N A, Frankel R B, Bazylinski D A, Maratea D, Rodgers C. 1990. Intercellular structure in a many-celled magnetotactic prokaryote. Archives of Microbiology, 154(1):18-22,
Shapiro O H, Hatzenpichler R, Buckley D H, Zinder S H, Orphan V J. 2011. Multicellular photo-magnetotactic bacteria. Environmental Microbiology Report, 3(2):233-238,
Simmons S L, Sievert S M, Frankel R B, Bazylinski D A, Edwards K J. 2004. Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Applied and Environmental Microbiology, 70(10):6230-6239,
Sobrinho R L, Lins U, Bernardes M C. 2011. Geochemical characteristics related to the gregite-producing multicellular magnetotactic prokaryote Candidatus Magnetoglobus multicellularis in a hypersaline lagoon. Geomicrobiology Journal, 28(8):705-713,
Wang H Z, Zhang X. 2017. Magnetic fields and reactive oxygen species. International Journal of Molecular Sciences, 18(10):2175,
Zhang R, Chen Y R, Du H J, Zhang W Y, Pan H M, Xiao T, Wu L F. 2014a. Characterization and phylogenetic identification of a species of spherical multicellular magnetotactic prokaryotes that produces both magnetite and greigite crystals. Research in Microbiology, 165(7):481-489,
Zhang S D, Petersen N, Zhang W J, Cargou S, Ruan J F, Murat D, Santini C L, Song T, Kato T, Notareschi P, Li Y, Namba K, Gué A M, Wu L F. 2014b. Swimming behaviour and magnetotaxis function of the marine bacterium strain MO-1. Environmental Microbiology Report, 6(1):14-20,
Zhang W J, Zhang S D, Wu L F. 2017. Measurement of freeswimming motility and magnetotactic behavior of Magnetococcus massalia Strain MO-1. Methods in Molecular Biology (Clifton, N. J.), 1593:305-320,
Zhou K, Pan H M, Zhang S D, Yue H D, Xiao T, Wu L F. 2011. Occurrence and microscopic analyses of multicellular magnetotactic prokaryotes from coastal sediments in the Yellow Sea. Chinese Journal of Oceanology and Limnology, 29(2):246-251,
Zhou K, Zhang W Y, Pan H M, Li J H, Yue H D, Xiao T, Wu L F. 2013. Adaptation of spherical multicellular magnetotactic prokaryotes to the geochemically variable habitat of an intertidal zone. Environmental Microbiology, 15(5):1595-1605,
Zhou K, Zhang W Y, Zhang K Y, Pan H M, Zhang S D, Zhang W J, Yue H D, Li Y, Xiao T, Wu L F. 2012. A novel genus of multicellular magnetotactic prokaryotes from the Yellow Sea. Environmental Microbiology, 14(2):405-413,
Zhu K L, Pan H M, Li J H, Zhang K Y, Zhang S D, Zhang W Y, Zhou K, Yue H D, Pan Y X, Xiao T, Wu L F. 2010. Isolation and characterization of a marine magnetotactic spirillum axenic culture QH-2 from an intertidal zone of the China Sea. Research in Microbiology, 161(4):276-283,
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