Comparative genomic analysis of magnetotactic bacteria from the Deltaproteobacteria provides new insights into magnetite and greigite magnetosome genes required for magnetotaxis

Summary Magnetotactic bacteria (MTB) represent a group of diverse motile prokaryotes that biomineralize magnetosomes, the organelles responsible for magnetotaxis. Magnetosomes consist of intracellular, membrane‐bounded, tens‐of‐nanometre‐sized crystals of the magnetic minerals magnetite (Fe3O4) or g...

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Published inEnvironmental microbiology Vol. 15; no. 10; pp. 2712 - 2735
Main Authors Lefèvre, Christopher T., Trubitsyn, Denis, Abreu, Fernanda, Kolinko, Sebastian, Jogler, Christian, de Almeida, Luiz Gonzaga Paula, de Vasconcelos, Ana Tereza R., Kube, Michael, Reinhardt, Richard, Lins, Ulysses, Pignol, David, Schüler, Dirk, Bazylinski, Dennis A., Ginet, Nicolas
Format Journal Article
LanguageEnglish
Published Oxford Blackwell Publishing Ltd 01.10.2013
Blackwell
Wiley Subscription Services, Inc
Subjects
Animal, plant and microbial ecology
Bacteriology
Biological and medical sciences
Conserved Sequence
Crystals
Deltaproteobacteria - classification
Deltaproteobacteria - genetics
Ferrosoferric Oxide
Fundamental and applied biological sciences. Psychology
General aspects
Genes
Genome, Bacterial - genetics
Iron
Magnetics
Magnetosomes - genetics
Magnetospirillum
Microbial ecology
Microbiology
Miscellaneous
Molecular Sequence Data
Multigene Family - genetics
Phylogeny
Sulfides
Magnetosome
Bacteria
Gene
Genomics
Magnetotaxis
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Summary:Summary Magnetotactic bacteria (MTB) represent a group of diverse motile prokaryotes that biomineralize magnetosomes, the organelles responsible for magnetotaxis. Magnetosomes consist of intracellular, membrane‐bounded, tens‐of‐nanometre‐sized crystals of the magnetic minerals magnetite (Fe3O4) or greigite (Fe3S4) and are usually organized as a chain within the cell acting like a compass needle. Most information regarding the biomineralization processes involved in magnetosome formation comes from studies involving Alphaproteobacteria species which biomineralize cuboctahedral and elongated prismatic crystals of magnetite. Many magnetosome genes, the mam genes, identified in these organisms are conserved in all known MTB. Here we present a comparative genomic analysis of magnetotactic Deltaproteobacteria that synthesize bullet‐shaped crystals of magnetite and/or greigite. We show that in addition to mam genes, there is a conserved set of genes, designated mad genes, specific to the magnetotactic Deltaproteobacteria, some also being present in Candidatus Magnetobacterium bavaricum of the Nitrospirae phylum, but absent in the magnetotactic Alphaproteobacteria. Our results suggest that the number of genes associated with magnetotaxis in magnetotactic Deltaproteobacteria is larger than previously thought. We also demonstrate that the minimum set of mam genes necessary for magnetosome formation in Magnetospirillum is also conserved in magnetite‐producing, magnetotactic Deltaproteobacteria. Some putative novel functions of mad genes are discussed.
Bibliography:ANR-P2N entitled MEFISTO
Fondation pour la Recherche Médicale - No. SPF20101220993
US National Science Foundation (NSF) - No. EAR-0920718
ark:/67375/WNG-X5T5R6QM-N
ArticleID:EMI12128
Brazilian CNPq/FAPERJ/CAPES
Supplementary information Fig. S1. Phylogenetic positions of magnetotactic Deltaproteobacteria. Phylogenetic tree, based on 16S rRNA gene sequences, showing the positions of the magnetotactic Deltaproteobacteria under study (bold) including Desulfovibrio magneticus, strain FH-1, strain ML-1, Candidatus Desulfamplus magnetomortis and Ca. Magnetoglobus multicellularis compared with magnetotactic bacteria from other classes or phylum (grey). Bootstrap values (higher than 50) at nodes are percentages of 100 replicates. Accession numbers are given in parentheses. Bar represents 5% sequence divergence.Fig. S2. Multiple sequence alignment of MamL homologues found in magnetotactic Alpha- and Deltaproteobacteria.Fig. S3. Phylogenetic tree based on amino acid sequences of the CDF proteins MamM and MamB, involved in magnetosome formation. The FieF protein from Escherichia coli K12 was used as an out-group. Phylogenetic reconstruction was based on maximum likelihood algorithm. Bar represents the percentage of sequence divergence.Fig. S4. Representation of the MamT* protein found in Candidatus Desulfamplus magnetomortis. MamT* appears to be a composite of 5 proteins (MamP1, MamT, OMM_15, OMM_14 and OMM_13) present in the greigite gene cluster of Ca. Magnetoglobus multicellularis.Table S1. Homologues of the Mad proteins of the magnetotactic Nitrospirae Candidatus Magnetobacterium bavaricum from Ca. Desulfamplus magnetomortis strain BW-1, Desulfovibrio magneticus strain RS-1, strains FH-1, ML-1 and Ca. Magnetoglobus multicellularis. Proteins are classified in the order they appear in the genome of Ca. M. bavaricum (% coverage, e-value, maximum identity).Table S2. Magnetosome genes present in the putative magnetosome gene islands of different cultured magnetotactic bacteria of the Alphaproteobacteria class that biomineralize cuboctahedral or elongated prismatic magnetite magnetosomes.Table S3. Magnetosome genes present in the putative magnetite gene cluster of different cultured magnetotactic bacteria of the Deltaproteobacteria class that biomineralize bullet-shaped magnetite magnetosomes.Supporting Information
Max-Planck society
Deutsche Forschungsgemeinschaft - No. DFG Schu1080/11-1
istex:DB88DA712A5413801895CBDD55A5E68508D08B76
ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ISSN:1462-2912
1462-2920
DOI:10.1111/1462-2920.12128