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Magnetotactic Bacteria

Published on 26 April 2019

Chercheurs: Damien FAIVRE, Christopher LEFEVRE, Pascal ARNOUX & David PIGNOL

Techniciens/Ingénieurs: Géraldine ADRYANCZYK, Béatrice ALONSO & Sandra PREVERAL

Doc​: Anissa DIEUDONNE, François MATHON

PostDoc: Caroline MONTEIL

Emiritus researcher: Michel PEAN

Magnetotactic bacteria (MTB) are aquatic prokaryotes, able to swim along the lines of the geomagnetic field. This unique behavior is made possible thanks to the alignment in the cytoplasm of specific magnetic organites, the magnetosomes. These magnetosomes are protein-lipid vesicles which encapsulate a magnetic crystal made of magnetite (Fe3O4) or greigite (Fe3S4) and whose size is around 50 nm. The biosynthesis of magnetosomes, their alignment within the cell as well as the nanocrystal biomineralization process are under the control of a group of gene encoding proteins associated with the magnetosomes. The  mechanisms involved in the synthesis of magnetosome remain poorly understood, and among  proteins found in all MTBs and only in them, original functions are still to be discovered.​ Our lab has become one of the leading groups  in deciphering this puzzling metal biomineralization process by combining comparative genomics with molecular approaches

Biodiversity, comparative genomics and genetics

Magnetotactic bacteria (MTB) represent a very diverse group of prokaryotes that do not form a separate branch in the tree of life but are rather spread in three different phyla: Proteobacteria, Nitrospirae and Omnitrophica. MTB diversity is still under-evaluated and our group contributed in the last period to the isolation and description of several new MTB strains from environmental samplings. Using comparative genomic analysis applied to various cultured or uncultured species, we were able (i) to decipher essential genes for magnetosome formation based on their conservation in the different groups of MTB, ii) to evidence genes specifically involved in controlling the shape of the biomineralized iron-rich particles, iii) to propose hypothesis on the historical evolution of magnetosomes, (iv) to describe original bacterial functions in MTB related to aero- magneto- taxis and cellular division.  In this topic, a pioneering result obtained in the last years was the isolation in pure culture of the first magnetite (iron oxide) and greigite (iron sulfur) producer (BW-1), a discovery published in Science in 2011. The genome of this strain is now completely sequenced  which paves the way to the full characterization of the genetic and environmental determinants controlling the chemical composition of the biomineralized crystal.

 

Mam proteins involved in the biogenesis of magnetosomes. 

A large genomic island, conserved among magnetotactic bacteria, contains genes potentially involved in magnetosome formation, most of them encoding proteins of unknown function. We deciphered in the last period original protein functions required for magnetosome alignment and magnetite biomineralization. We are interested in the function of MamK, an "actin-like" responsible for the alignment of the magnetosomes chain (5,13). Transcriptional regulator controlling the synthesis of the organelle has also been characterized (12). Electron transfer mechanisms required for the biomineralization of magnetite nanocrystals are also addressed by the study of specific redox proteins. Thus, we were able to identify 4 Mam proteins (MAMP, T, X and E) that contain a new type of single-heme cytochrome specific to MTBs and coined the magnetochrome (6, 10). We have characterized MamP in details: it is an iron oxidase whose activity is required to control the redox balance of iron. The structure of MamP also highlights the unique folding of the magnetochro​me domain that represents the smaller mono-heme cytochrome described to date (9).​​

 
 
 
Diversity of magnetotactic bacteria
Crédit : Christopher Lefèvre/ CEA
 
 
 
 
 
                       

MamP is anironoxidase whose activity is required to control the redox balanceof iron.  

      Collaborators
      ​​​
      • France: N. Menguy, K. Benzerara, E. Duprat (UPMC, Paris), F. Guyot (MNHN, Paris), V. Busigny (IPGP, Paris), S. Mériaux (Neurospin, Saclay), C. Wilhelm (MSC, Paris).
      • USA: A. komeili (UC Berkeley), D. Bazylinski (UNLV, Las Vegas)
      • Israel: R. Zarivach (University of the Negev, Beer-Sheva)
      • Germany:  D. Schüler (University of Bayreuth)
      • South Africa: M. Tuffin (IMBM, Cape Town), E. Van Zyl (University of Pretoria)
      • New Zealand: R. Weld (Lincoln Agritech  Ltd)

    Fundings

    ANR Tremplin-ERC BIOMAGNET; 2017-2018, coordinator C. Lefevre

    Ministry of Business, Innovation and Employment (MBIE) Nouvelle Zélande, 2018- 2019, collaborator C. Lefevre (coordinator R. Weld)

    Defi ISOTOP-CNRS, 2018, coordinator C. lefevre

    ANR SIGMAG, 2018-2021, coordinators V. Busigny and D. Pignol

     

     

    Selected publications​​​​

    Applied research

    Plan Sangnier A, Preveral S, Curcio A, K A Silva A, Lefèvre CT, Pignol D, Lalatonne Y, Wilhelm C (2018) Targeted thermal therapy with genetically engineered magnetite magnetosomes@RGD: Photothermia is far more efficient than magnetic hyperthermia. J Control Release. 279:271-281. doi: 10.1016/j.jconrel.2018.04.036

    Smit BA, Van Zyl E, Joubert JJ, Meyer W, Prévéral S, Lefèvre CT, Venter SN (2018) Magnetotactic bacteria used to generate electricity based on Faraday's law of electromagnetic induction. Let Appl Microbiol. 66:362-367. doi: 10.1111/lam.12862

    Boucher M, Geffroy F, Prévéral S, Bellanger L, Selingue E, Adryanczyk-Perrier G, Péan M, Lefèvre CT, Pignol D, Ginet N, Mériaux S. (2017) Genetically tailored magnetosomes used as MRI probe for molecular imaging of brain tumor. Biomaterials. 121:167-178 doi: 10.1016/j.biomaterials.2016.12.013.

     

    Biodiversity and evolution of magnetotactic bacteria

     

    Lefèvre CT, Menguy N, Abreu F, Lins U, Pósfai M, Prozorov T, Pignol D, Frankel RB, Bazylinski DA (2011A Cultured Greigite-Producing Magnetotactic Bacterium in a Novel Group of Sulfate-Reducing BacteriaScience 334(6063):1720-3.

    Lefèvre CT, Trubitsyn D, Abreu F, Kolinko S, Gonzaga Paula de Almeida L, R de Vasconcelos AT, Kube M, Reinhardt R, Schüler D, Lins U, Pignol D, Bazylinski D, Ginet N (2013"Comparative Genomics Analysis of Magnetotactic Bacteria of the Deltaproteobacteria Give a New Insight into the Magnetite and Greigite Magnetosome Genes Required for Magnetotaxis" Env Microb doi: 10.1111/1462-2920.12128

    Rivas-Lamelo S, Benzerara K, Lefèvre CT, Monteil CL, Jézéquel D, Menguy N, Viollier E, Guyot F, Férard C, Poinsot M, Skouri-Panet F, Trcera N, Miot J, Duprat E (2017) Magnetotactic bacteria as a new model for P sequestration in the ferruginous Lake Pavin. Geochem Persp Let. 5:35-41.

    Monteil CL, Menguy N, Prévéral S, Warren A, Pignol D, Lefèvre CT (2018) Accumulation and dissolution of magnetite crystals in a magnetically responsive ciliate. Appl Environ Microbiol. e02865-17. doi: 10.1128/AEM.02865-17


    Biomineralization

    Siponen M, Adryanczyk G, Ginet N, Arnoux P, Pignol D (2012An Electron Transfer chain for Magnetotatic Bacteria Organelle Formation.Biochem Soc Trans 1;40(6):1319-23.

    Abreu N, Mannoubi S, Ozyamak E, Pignol DGinet N, Komeili A. (2014) The interplay between two bacterial actin homologs, MamK and MamK-like, is required for the alignment of magnetosome organelles in Magnetospirillum magneticum AMB-1 J. Bacteriol  Sep 1;196(17):3111-21. doi: 10.1128/JB.01674-14. Epub 2014

    LiY, Sabaty M, Borg S, Silva KT, Pignol D, Schüler D. (2014) The oxygen sensor MgFnr controls magnetite biomineralization by regulation of denitrification in Magnetospirillum gryphiswaldenseBMC Microbiology Jun 10;14:153. doi: 10.1186/1471-2180-14-153

     

    Microswimmers

    Lefèvre C.T., Bennet M., Klumpp S. & Faivre D. (2015) « Positioning the flagellum at the center to combine bacterial division with magnetic polarity » mBio    Feb 24;6(2). pii: e02286-14. doi: 10.1128/mBio.02286

    Lefèvre CT, Bennet M, Landau L, Vach P, Pignol D, Bazylinski D, Frankel R, Klumpp S, Faivre D. (2014) Diversity of magneto-aerotactic behaviours and oxygen sensing mechanisms in cultured magnetotactic bacteria . Biophysical Journal 15;107(2):527-38. doi: 10.1016/j.bpj.2014.05.043

     

    Review

    Klumpp S, Lefèvre CT, Bennet M, Faivre D (2019) Swimming with magnets: From biological organisms to synthetic devices. Physics Reports 789:1–54 doi.org/10.1016/j.physrep.2018.10.007

    Lefèvre CT, Bazylinski DA (2013) Ecology, diversity, and evolution of magnetotactic bacteria. Microbiol Mol Biol. 77:497-526. doi: 10.1128/MMBR.00021-13