Newly Isolated but Uncultivated Magnetotactic Bacterium of the Phylum Nitrospirae from Beijing, China

ABSTRACT Magnetotactic bacteria (MTB) in the phylum Nitrospirae synthesize up to hundreds of intracellular bullet-shaped magnetite magnetosomes. In the present study, a watermelon-shaped magnetotactic bacterium (designated MWB-1) from Lake Beihai in Beijing, China, was characterized. This uncultivated microbe was identified as a member of the phylum Nitrospirae and represents a novel phylogenetic lineage with ≥6% 16S rRNA gene sequence divergence from all currently described MTB. MWB-1 contained 200 to 300 intracellular bullet-shaped magnetite magnetosomes and showed a helical swimming trajectory under homogeneous magnetic fields; its magnetotactic velocity decreased with increasing field strength, and vice versa. A robust phylogenetic framework for MWB-1 and all currently known MTB in the phylum Nitrospirae was constructed utilizing maximum-likelihood and Bayesian algorithms, which yielded strong evidence that the Nitrospirae MTB could be divided into four well-supported groups. Considering its population densities in sediment and its high numbers of magnetosomes, MWB-1 was estimated to account for more than 10% of the natural remanent magnetization of the surface sediment. Taken together, the results of this study suggest that MTB in the phylum Nitrospirae are more diverse than previously realized and can make important contributions to the sedimentary magnetization in particular environments.

[1]  Wei Lin,et al.  Reduced efficiency of magnetotaxis in magnetotactic coccoid bacteria in higher than geomagnetic fields. , 2009, Biophysical journal.

[2]  M. Winklhofer,et al.  SPATIAL ARRANGEMENT OF CHAINS OF MAGNETOSOMES IN MAGNETOTACTIC BACTERIA , 1996 .

[3]  Damien Faivre,et al.  Magnetotactic bacteria and magnetosomes. , 2008, Chemical reviews.

[4]  Yongxin Pan,et al.  The detection of bacterial magnetite in recent sediments of Lake Chiemsee (southern Germany) , 2005 .

[5]  Long-Fei Wu,et al.  Isolation and characterization of a magnetotactic bacterial culture from the Mediterranean Sea. , 2009, Environmental microbiology.

[6]  R. Kopp,et al.  The identification and biogeochemical interpretation of fossil magnetotactic bacteria , 2008 .

[7]  Yongxin Pan,et al.  Temporal variation of magnetotactic bacterial communities in two freshwater sediment microcosms. , 2010, FEMS microbiology letters.

[8]  D. Schüler,et al.  Diversity analysis of magnetotactic bacteria in Lake Miyun, northern China, by restriction fragment length polymorphism. , 2009, Systematic and applied microbiology.

[9]  R. Blakemore.  Magnetotactic bacteria , 1975, Science.

[10]  D. Schüler,et al.  Cultivation-independent characterization of 'Candidatus Magnetobacterium bavaricum' via ultrastructural, geochemical, ecological and metagenomic methods. , 2010, Environmental microbiology.

[11]  D. Schüler,et al.  Metagenomic Analysis Reveals Unexpected Subgenomic Diversity of Magnetotactic Bacteria within the Phylum Nitrospirae , 2010, Applied and Environmental Microbiology.

[12]  Yongxin Pan,et al.  Does capillary racetrack-based enrichment reflect the diversity of uncultivated magnetotactic cocci in environmental samples? , 2008, FEMS microbiology letters.

[13]  Wolfgang Wiltschko,et al.  Magnetoreception , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[14]  K. Schleifer,et al.  Dominating Role of an Unusual Magnetotactic Bacterium in the Microaerobic Zone of a Freshwater Sediment , 1993, Applied and environmental microbiology.

[15]  D. Schüler,et al.  Toward Cloning of the Magnetotactic Metagenome: Identification of Magnetosome Island Gene Clusters in Uncultivated Magnetotactic Bacteria from Different Aquatic Sediments , 2009, Applied and Environmental Microbiology.

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

[17]  R. Frankel,et al.  Culture-independent characterization of a novel, uncultivated magnetotactic member of the Nitrospirae phylum. , 2011, Environmental microbiology.

[18]  Erko Stackebrandt,et al.  Taxonomic Note: A Place for DNA-DNA Reassociation and 16S rRNA Sequence Analysis in the Present Species Definition in Bacteriology , 1994 .

[19]  D. Schüler,et al.  Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branching Nitrospira phylum , 2010, Proceedings of the National Academy of Sciences.

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

[21]  H. L. Barros,et al.  Study of the motion of magnetotactic bacteria , 1995, European Biophysics Journal.

[22]  A. Tornheim,et al.  Observation of magnetoreceptive behavior in a multicellular magnetotactic prokaryote in higher than geomagnetic fields. , 2005, Biophysical journal.

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

[24]  Ulysses Lins,et al.  Moderately Thermophilic Magnetotactic Bacteria from Hot Springs in Nevada , 2010, Applied and Environmental Microbiology.

[25]  Yoshio Umezawa,et al.  A high-throughput screening of genes that encode proteins transported into the endoplasmic reticulum in mammalian cells , 2005, Nucleic acids research.

[26]  Dirk Schüler,et al.  Genomics, genetics, and cell biology of magnetosome formation. , 2009, Annual review of microbiology.

[27]  E. Larquet,et al.  Transmission electron microscopy study of magnetites in a freshwater population of magnetotactic bacteria , 2007 .

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

[29]  Yongxin Pan,et al.  Uncultivated Magnetotactic Cocci from Yuandadu Park in Beijing, China , 2009, Applied and Environmental Microbiology.

[30]  R. Che,et al.  Biomineralization, crystallography and magnetic properties of bullet-shaped magnetite magnetosomes in giant rod magnetotactic bacteria , 2010 .

[31]  Yongxin Pan,et al.  Rock magnetic properties of uncultured magnetotactic bacteria , 2005 .

[32]  Yongxin Pan,et al.  Combined Approaches for Characterization of an Uncultivated Magnetotactic coccus from Lake Miyun near Beijing , 2009 .

[33]  T. Matsunaga,et al.  A morphological classification of bacteria containing bullet-shaped magnetic particles , 1994 .

[34]  David L. Wheeler,et al.  GenBank , 2015, Nucleic Acids Res..

[35]  K. Kogure,et al.  Bacterial motility: links to the environment and a driving force for microbial physics. , 2006, FEMS microbiology ecology.

[36]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[37]  Yongxin Pan,et al.  A biogeographic distribution of magnetotactic bacteria influenced by salinity , 2011, The ISME Journal.

[38]  Stephen Mann,et al.  Ultrastructure and characterization of anisotropic magnetic inclusions in magnetotactic bacteria , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[39]  M. Winklhofer,et al.  Pulsed-field-remanence measurements on individual magnetotactic bacteria , 2002 .

[40]  H. Vali,et al.  Magnetic Bacteria in Lake Sediments , 1989 .

[41]  R. Frankel,et al.  Novel magnetite-producing magnetotactic bacteria belonging to the Gammaproteobacteria , 2011, The ISME Journal.

[42]  Thomas Huber,et al.  Bellerophon: a program to detect chimeric sequences in multiple sequence alignments , 2004, Bioinform..

[43]  D. Schüler,et al.  Diversity and vertical distribution of magnetotactic bacteria along chemical gradients in freshwater microcosms. , 2005, FEMS microbiology ecology.

[44]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[45]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[46]  J. Kirschvink.  Magnetite biomineralization and geomagnetic sensitivity in higher animals: an update and recommendations for future study. , 1989, Bioelectromagnetics.

[47]  Wei Qian,et al.  Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. , 2000, Molecular biology and evolution.

[48]  M. Farina,et al.  Electron Spectroscopic Imaging of Magnetotactic Bacteria: Magnetosome Morphology and Diversity , 2000, Microscopy and Microanalysis.

[49]  Hojatollah Vali,et al.  Magnetotactic bacteria and their magnetofossils in sediments , 1987 .

[50]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[51]  D. Weiss,et al.  Movement of magnetic bacteria in time-varying magnetic fields , 1994, Journal of Fluid Mechanics.

[52]  K. Edwards,et al.  Geobiology of Magnetotactic Bacteria , 2006 .

[53]  D. Schüler,et al.  Diversity and Taxonomy of Magnetotactic Bacteria , 2006 .

[54]  D A Stahl,et al.  Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology , 1990, Journal of bacteriology.

[55]  R. Amann,et al.  Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes , 2001 .