Aquatic Microbiology

Intracellular biomineralization in bacteria Wei Lin, Karim Benzerara, Damien Faivre and Yongxin Pan

Journal Name:

Frontiers in Microbiology

ISSN:

1664-302X

Article type:

Editorial Article

Received on:

14 May 2014

Accepted on:

28 May 2014

Provisional PDF published on:

28 May 2014

www.frontiersin.org:

www.frontiersin.org

Citation:

Lin W, Benzerara K, Faivre D and Pan Y(2014) Intracellular biomineralization in bacteria. Front. Microbiol. 5:293. doi:10.3389/fmicb.2014.00293

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Intracellular biomineralization in bacteria

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Wei Lin1,2*, Karim Benzerara3*, Damien Faivre4* and Yongxin Pan1,2*

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and Geophysics, Chinese Academy of Sciences, Beijing 100029, China

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Beijing 100029, China

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Biogeomagnetism Group, PGL, Key Laboratory of Earth and Planetary Physics, Institute of Geology

France-China Bio-Mineralization and Nano-Structures Laboratory, Chinese Academy of Sciences,

Institut de Minéralogie, de Physique des Matériaux, et de Cosmochimie (IMPMC). Sorbonne

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Universités - UPMC Univ Paris 06, CNRS UMR 7590, MNHN, IRD UMR 206, 4 Place Jussieu, 75005

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Paris, France

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14424 Potsdam, Germany

Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Science Park Golm,

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*Correspondence: [email protected] (W.L.), [email protected] (K.B.),

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[email protected] (D.F.), and [email protected] (Y.P.)

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Microorganisms have populated the Earth for billions of years and their activities are

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important forces shaping our planetary environments through biogeochemical cycles.

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In particular, microbial biomineralization that selectively take up environmental

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elements and deposit minerals either intracellularly or extracellularly is of great

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interest, because these processes play vital roles in the global cycles of numerous

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elements, such as Fe, Mn, Ca, As, O, S, and P, etc. Biominerals, the products of

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biomineralization, not only serve as important biosignatures for the search of traces of

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past life and the reconstruction of ancient environments but also have many important

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commercial applications.

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Recent advances in sequencing technologies, molecular analyses and approaches for assaying protein functions pave the way for rapid progress in microbial

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biomineralization research. The objective of this research topic is to highlight the

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latest advances in our understanding of intracellular biomineralization in bacteria,

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with a focus on the magnetotactic bacteria (MTB), a group of phylogenetically

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diverse microbes synthesizing magnetic minerals of magnetite (Fe3O4) and/or greigite

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(Fe3S4) magnetosomes in cells. Magnetosomes are generally less than 150 nm in

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length, covered by lipid bilayer membrane and organized into one or multiple chain

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structures that act like a compass needle to facilitate the navigation of MTB using the

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Earth’s magnetic field. The uniform nano sizes, superior magnetic properties and

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perfect chain arrangement suggest a strict genetic control of magnetosome synthesis

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in MTB cells, which provides an attractive model system for investigating the

 

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mechanisms of bacterial intracellular biomineralization. This research topic provides

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a selection of interesting and challenging topics of research on the diversity, ecology,

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evolution, genomics and biochemistry of MTB. The applications of magnetosomes in

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biotechnology and paleoenvironmental reconstruction are also covered here.

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This research topic begins with a review on the relationship between all known

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magnetosome crystal habits and the phylogenetic affiliations of MTB (Pósfai et al.,

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2013), which serves as guide to better understand the evolutionary history of

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magnetosome formation and magnetotaxis in MTB. Following this review, Morillo et

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al. (2014) report the first cultivation and genomic characterization of a south-seeking

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Alphaproteobacteria magnetotactic coccus Magnetofaba australis strain IT-1 from

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the Southern Hemisphere. The findings of their study provide important clues to the

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evolution of magnetotactic Alphaproteobacteria. Oestreicher et al. (2013) examine

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the morphological and phylogenetic diversity of MTB in a freshwater lake containing

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microbialites. Their results raise the interesting question of whether MTB

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magnetosomes could be preserved in microbialites and serve as robust biomarkers.

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Kong et al. (2014) investigate the swimming behavior of a rod-shaped magnetotactic

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Nitrospirae, with hundreds bullet-shaped magnetite magnetosomes per cell, under the

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influence of a magnetic field. The authors have developed the first mathematical

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model to describe both the magnetotactic motion and orientation of this rod-shaped

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bacterium.

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Three articles deal with the mechanisms of magnetosome biomineralization.

 

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Rahn-Lee and Komeili (2013) summarize the recent advances in the molecular

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mechanisms of magnetosome synthesis and discuss their implications for

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understanding bacterial intracellular biomineralization in general. Arnoux et al. (2014)

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focus on those magnetosome-associated proteins containing a c-type cytochrome

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domain. The authors evaluate the evolution of these proteins, and a model is proposed,

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which offers a different perspective on the evolution of magnetosome formation.

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Through bioinformatics approaches, Nudelman and Zarivach (2014) perform 3D

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structural predictions of all known magnetosome-associated proteins in

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Magnetospirillum gryphiswaldense strain MSR-1. Their results propose a

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comprehensive review of the functional features of biomineralization proteins.

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Three papers explore the effects of environmental factors on magnetosome

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formation and their implications for the ancient environment. Moisescu et al. (2014)

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review the recent advances in understanding the effects of chemical and physical

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factors on magnetosome synthesis. They also discuss the potential of magnetosomes

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as biomarkers for ancient life and the role of MTB in iron cycling. The study by

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Wang et al. (2013) focuses on the influence of ultraviolet-B radiation on

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Magnetospirillum magneticum strain AMB-1. The authors note that ultraviolet-B

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radiation could affect both cell growth and magnetite synthesis, and suggest that

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magnetosomes may have evolutionary benefits for the survival of MTB under

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extreme environments. A paleo- and rock-magnetic study of marine sediments from

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the Guadalquivir Basin, Spain by Larrasoaña et al. (2014) reveals dominance of fossil

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magnetosome chains in sediments. Their results indicate that fossil magnetosomes

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could provide important paleomagnetic and paleoenvironmental information.

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Finally, the articles by Xu et al. (2014) and Yang et al. (2013) focus on the

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strain MSR-1. Xu et al. (2014) report the expression of staphylococcal protein A on

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the surface of extracted magnetosomes. These functionalized magnetosomes are

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capable of efficiently detecting pathogenic Vibrio parahaemolyticus. Yang et al.

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(2013) perform experiments with a large-scale culture of M. gryphiswaldense and

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identify the key time point for cell growth as well as magnetosome formation. The high-yield production achieved in their study suggests great opportunities for further

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applications of magnetite magnetosomes in various commercial fields.

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reviewers involved in processing these papers. We hope that this research topic will

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provide an in-depth exploration of microbial biomineralization and stimulate new

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investigators and more questions within this fascinating field.

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References

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Arnoux, P., Siponen, M.I., LefèVre, C.T., Ginet, N., and Pignol, D. (2014). Structure and evolution of the magnetochrome domains: no longer alone. Front. Microbiol. 5, 117. doi: 10.3389/fmicb.2014.00117. Kong, D., Lin, W., Pan, Y., and Zhang, K. (2014). Swimming motion of rod-shaped magnetotactic bacteria: the effects of shape and growing magnetic moment. Front. Microbiol. 5, 8. doi: 10.3389/fmicb.2014.00008. LarrasoañA, J.C., Liu, Q., Hu, P., Roberts, A.P., Mata, P., Civis, J., Sierro, F.J., and PéRez-Asensio, J.N. (2014). Paleomagnetic and paleoenvironmental implications of magnetofossil occurrences in late Miocene marine sediments from the Guadalquivir Basin, SW Spain. Front. Microbiol. 5, 71. doi: 10.3389/fmicb.2014.00071.  

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121   We are very grateful to all the authors for their contributions and to all of the

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119   production and application of magnetosomes from Magnetospirillum gryphiswaldense

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Moisescu, C., Ardelean, I., and Benning, L.G. (2014). The effect and role of environmental conditions on magnetosome synthesis. Front. Microbiol. 5, 49. doi: 10.3389/fmicb.2014.00049. Morillo, V., Abreu, F., Araujo, A.C., Almeida, L.G.P.D., Prast, A.E., Farina, M., Vasconcelos, A.T.R.D., Bazylinski, D.A., and Lins, U. (2014). Isolation, cultivation and genomic analysis of magnetosome biomineralization genes of a new genus of South-seeking magnetotactic cocci within the Alphaproteobacteria. Front. Microbiol. 5, 72. doi: 10.3389/fmicb.2014.00072. Nudelman, H., and Zarivach, R. (2014). Structure prediction of magnetosome-associated proteins. Front. Microbiol. 5, 9. doi: 10.3389/fmicb.2014.00009. Oestreicher, Z., Lower, S.K., Rees, E., Bazylinski, D.A., and Lower, B.H. (2013). Magnetotactic bacteria from Pavilion Lake, British Columbia. Front. Microbiol. 4, 406. doi: 10.3389/fmicb.2013.00406. Pósfai, M., Lefèvre, C., Trubitsyn, D., Bazylinski, D.A., and Frankel, R. (2013). Phylogenetic significance of composition and crystal morphology of magnetosome minerals. Front. Microbiol. 4, 344. doi: 10.3389/fmicb.2013.00344. Rahn-Lee, L., and Komeili, A. (2013). The magnetosome model: insights into the mechanisms of bacterial biomineralization. Front. Microbiol. 4, 352. doi: 10.3389/fmicb.2013.00352. Wang, Y., Lin, W., Li, J., and Pan, Y. (2013). Changes of cell growth and magnetosome biomineralization in Magnetospirillum magneticum AMB-1 after ultraviolet-B irradiation. Front. Microbiol. 4, 397. doi: 10.3389/fmicb.2013.00397. Xu, J., Hu, J., Liu, L., Li, L., Wang, X., Zhang, H., Jiang, W., Tian, J., Li, Y., and Li, J. (2014). Surface expression of protein A on magnetosomes and capture of pathogenic bacteria by magnetosome/antibody complexes. Front. Microbiol. 5, 136. doi: 10.3389/fmicb.2014.00136. Yang, J., Li, S., Huang, X., Tang, T., Jiang, W., Zhang, T., and Li, Y. (2013). A key time point for cell growth and magnetosome synthesis of Magnetospirillum gryphiswaldense based on real-time analysis of physiological factors. Front. Microbiol. 4, 210. doi: 10.3389/fmicb.2013.00210.

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