Isolation and characterization of a magnetotactic bacterial culture from the Mediterranean Sea.

The widespread magnetotactic bacteria have the peculiar capacity of navigation along the geomagnetic field. Despite their ubiquitous distribution, only few axenic cultures have been obtained worldwide. In this study, we reported the first axenic culture of magnetotactic bacteria isolated from the Mediterranean Sea. This magneto-ovoid strain MO-1 grew in chemically defined O(2) gradient minimal media at the oxic-anoxic transition zone. It is phylogenetically related to Magnetococcus sp. MC-1 but might represent a novel genus of Proteobacteria. Pulsed-field gel electrophoresis analysis indicated that the genome size of the MO-1 strain is 5 ± 0.5 Mb, with four rRNA operons. Each cell synthesizes about 17 magnetosomes within a single chain, two phosphorous-oxygen-rich globules and one to seven lipid storage granules. The magnetosomes chain seems to divide in the centre during cell division giving rise to two daughter cells with an approximately equal number of magnetosomes. The MO-1 cell possesses two bundles of seven individual flagella that were enveloped in a unique sheath. They swam towards the north pole with a velocity up to 300 μm per second with frequent change from right-hand to left-hand helical trajectory. Using a magneto-spectrophotometry assay we showed that MO-1 flagella were powered by both proton-motive force and sodium ion gradient, which is a rare feature among bacteria.

[1]  T. Matsunaga,et al.  Design and Application of a New Cryptic-Plasmid-Based Shuttle Vector for Magnetospirillum magneticum , 2003, Applied and Environmental Microbiology.

[2]  S. Fowler,et al.  Nile red: a selective fluorescent stain for intracellular lipid droplets , 1985, The Journal of cell biology.

[3]  J. Yonnet,et al.  Characterization of Mediterranean magnetotactic bacteria , 2007 .

[4]  R. Frankel,et al.  Electron microscopy study of magnetosomes in a cultured coccoid magnetotactic bacterium , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[5]  I. Fridovich,et al.  Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. , 1971, Analytical biochemistry.

[6]  Peter R. Buseck,et al.  Magnetite from magnetotactic bacteria; size distributions and twinning , 1998 .

[7]  Holger W. Jannasch,et al.  Anaerobic magnetite production by a marine, magnetotactic bacterium , 1988, Nature.

[8]  A. Steinbüchel,et al.  Neutral Lipid Bodies in Prokaryotes: Recent Insights into Structure, Formation, and Relationship to Eukaryotic Lipid Depots , 2005, Journal of bacteriology.

[9]  Long-Fei Wu,et al.  Characterization of a homogeneous taxonomic group of marine magnetotactic cocci within a low tide zone in the China Sea. , 2008, Environmental microbiology.

[10]  Long-Fei Wu,et al.  A simple and accurate method for quantification of magnetosomes in magnetotactic bacteria by common spectrophotometer. , 2007, Journal of biochemical and biophysical methods.

[11]  R. Blakemore,et al.  Magnetotactic bacteria , 1975, Science.

[12]  T. Lessie,et al.  Multiple replicons constituting the genome of Pseudomonas cepacia 17616 , 1994, Journal of bacteriology.

[13]  R. F. Gray,et al.  Physical and genetic characterization of the genome of Magnetospirillum magnetotacticum, strain MS-1. , 2001, Gene.

[14]  K. Edwards,et al.  South-Seeking Magnetotactic Bacteria in the Northern Hemisphere , 2006, Science.

[15]  D. DeRosier,et al.  A three-start helical sheath on the flagellar filament of Caulobacter crescentus , 1992, Journal of bacteriology.

[16]  S. Suerbaum,et al.  Ultrastructure and chemical analysis of Campylobacter pylori flagella , 1989, Journal of clinical microbiology.

[17]  Robert F. Butler,et al.  Theoretical single‐domain grain size range in magnetite and titanomagnetite , 1975 .

[18]  D. Schüler Magnetoreception and magnetosomes in bacteria , 2007 .

[19]  C. Emala,et al.  Invited review: bacterial flagellar sheaths: structures in search of a function. , 1983, Cell motility.

[20]  S. Giovannoni,et al.  High-Throughput Methods for Culturing Microorganisms in Very-Low-Nutrient Media Yield Diverse New Marine Isolates , 2002, Applied and Environmental Microbiology.

[21]  Toshifumi Sakaguchi,et al.  Magnetite formation by a magnetic bacterium capable of growing aerobically , 1991, Applied Microbiology and Biotechnology.

[22]  M. Farina,et al.  Ultrastructure and cytochemistry of lipid granules in the many-celled magnetotactic prokaryote, 'Candidatus Magnetoglobus multicellularis'. , 2008, Micron.

[23]  Isolation of magnetotactic bacterium WM-1 from freshwater sediment and phylogenetic characterization , 2007, Archives of Microbiology.

[24]  R. Thauer,et al.  A ‘capillary racetrack’ method for isolation of magnetotactic bacteria , 1987 .

[25]  D. Schüler,et al.  Comparative Genome Analysis of Four Magnetotactic Bacteria Reveals a Complex Set of Group-Specific Genes Implicated in Magnetosome Biomineralization and Function , 2007, Journal of bacteriology.

[26]  R. Frankel,et al.  Magnetosome formation in prokaryotes , 2004, Nature Reviews Microbiology.

[27]  R. Frankel,et al.  Magneto-aerotaxis in marine coccoid bacteria. , 1997, Biophysical journal.

[28]  H. Busse,et al.  Proposed minimal standards for the description of genera, species and subspecies of the Pasteurellaceae. , 2007, International journal of systematic and evolutionary microbiology.

[29]  C. Lemieux,et al.  A group I intron in the chloroplast large subunit rRNA gene of Chlamydomonas eugametos encodes a double-strand endonuclease that cleaves the homing site of this intron , 2004, Current Genetics.

[30]  M. Mandrand-Berthelot,et al.  Genetic and physiological characterization of new Escherichia coli mutants impaired in hydrogenase activity. , 1986, Biochimie.

[31]  H. Berg The rotary motor of bacterial flagella. , 2003, Annual review of biochemistry.

[32]  R S Wolfe,et al.  Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium , 1979, Journal of bacteriology.

[33]  I. Raška,et al.  Plain and Complex Flagella of Pseudomonas rhodos: Analysis of Fine Structure and Composition , 1974, Journal of bacteriology.

[34]  D. Schüler,et al.  The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense , 2002, International microbiology : the official journal of the Spanish Society for Microbiology.

[35]  Dirk SchA ler,et al.  Genetics and cell biologyofmagnetosomeformation in magnetotactic bacteria , 2008 .

[36]  L. McCarter Polar Flagellar Motility of theVibrionaceae , 2001, Microbiology and Molecular Biology Reviews.

[37]  D. Schüler,et al.  Combined Approach for Characterization of Uncultivated Magnetotactic Bacteria from Various Aquatic Environments , 2005, Applied and Environmental Microbiology.

[38]  D. Bazylinski,et al.  Genome Analysis of Several Marine, Magnetotactic Bacterial Strains by Pulsed-Field Gel Electrophoresis , 1999, Current Microbiology.

[39]  R. Blakemore,et al.  South-seeking magnetotactic bacteria in the Southern Hemisphere , 1980, Nature.

[40]  C. Santini,et al.  Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles , 2006, Proceedings of the National Academy of Sciences.

[41]  R. Blakemore,et al.  Magnetic Navigation in Bacteria , 1981 .

[42]  Atsushi Arakaki,et al.  Desulfovibrio magneticus sp. nov., a novel sulfate-reducing bacterium that produces intracellular single-domain-sized magnetite particles. , 2002, International journal of systematic and evolutionary microbiology.

[43]  Y. Imae,et al.  Polar and lateral flagellar motors of marine Vibrio are driven by different ion-motive forces , 1992, Nature.

[44]  P. Little Genome analysis , 1996 .

[45]  D. Schüler,et al.  Genetic Analysis of Magnetosome Biomineralization , 2006 .

[46]  J. Errington,et al.  A dynamic bacterial cytoskeleton. , 2003, Trends in cell biology.

[47]  T. Williams,et al.  Evidence for Autotrophy via the Reverse Tricarboxylic Acid Cycle in the Marine Magnetotactic Coccus Strain MC-1 , 2006, Applied and Environmental Microbiology.

[48]  D. Schüler,et al.  The Genus Magnetospirillum gen. nov. Description of Magnetospirillum gryphiswaldense sp. nov. and Transfer of Aquaspirillum magnetotacticum to Magnetospirillum magnetotacticum comb. nov. , 1991 .