DU Haijian, ZHANG Rui, ZHANG Wenyan, XU Cong, CHEN Yiran, PAN Hongmiao, ZHOU Ke, WU Long-fei, XIAO Tian. Characterization of uncultivated magnetotactic bacteria from the sediments of Yuehu Lake, China[J]. Acta Oceanologica Sinica, 2017, 36(2): 94-104. doi: 10.1007/s13131-017-0980-8
Citation: DU Haijian, ZHANG Rui, ZHANG Wenyan, XU Cong, CHEN Yiran, PAN Hongmiao, ZHOU Ke, WU Long-fei, XIAO Tian. Characterization of uncultivated magnetotactic bacteria from the sediments of Yuehu Lake, China[J]. Acta Oceanologica Sinica, 2017, 36(2): 94-104. doi: 10.1007/s13131-017-0980-8

Characterization of uncultivated magnetotactic bacteria from the sediments of Yuehu Lake, China

doi: 10.1007/s13131-017-0980-8
  • Received Date: 2015-11-04
  • Rev Recd Date: 2016-08-23
  • Marine magnetotactic bacteria were collected from the intertidal sediments of Yuehu Lake (China), where their abundance reached 103-104 ind./cm3. Diverse morphotypes of magnetotactic bacteria were observed, including cocci and oval, vibrio-, spirillum-, rod-, elliptical-, handle- and bar-shaped forms. The magnetococci were the most abundant, and had flagella arranged in parallel within a bundle. The majority of magnetosomes were arranged in one, two or multiple chains, although irregular arrangements were also evident. All the results of high-resolution transmission electron microscopy (HRTEM) analysis show that magnetosome crystals were composed of Fe3O4, and their morphology was specific to particular cell morphotypes. By the 16S rRNA gene sequence analysis, we found fourteen operational taxonomic units (OTUs) which were related to magnetotactic bacteria. Among these, thirteen belonged to the Alphaproteobacteria and one to the Gammaproteobacteria. Compared with known axenic and uncultured marine magnetotactic bacteria, the 16S rRNA gene sequences of most magnetotactic bacteria collected from the Yuehu Lake exhibited sequence identities ranging from 90.1% to 96.2% (<97%). The results indicate that microbial communities containing previously unidentified magnetotactic bacteria occur in the Yuehu Lake.
  • loading
  • Abreu F, Martins J L, Silveira T S, et al. 2007. ‘Candidatus magnetoglobus multicellularis’, a multicellular, magnetotactic prokaryote from a hypersaline environment. Int J Syst Evol Microbiol, 57(6):1318-1322
    Altschul S F, Madden T L, Schäffer A A, et al. 1997. Gapped BLAST and PSI-BLAST:a new generation of protein database search programs. Nucleic Acids Res, 25(17):3389-3402
    Amann R, Peplies J, Schüler D. 2006. Diversity and taxonomy of magnetotactic bacteria. In:Schüler D, ed. Magnetoreception and Magnetosomes in Bacteria:Microbiology Monographs. Berlin Heidelberg:Springer, 25-36
    Arakaki A, Nakazawa H, Nemoto M, et al. 2008. Formation of magnetite by bacteria and its application. J Roy Soc Interface, 5(26):977-999
    Balkwill D L, Maratea D, Blakemore R P. 1980. Ultrastructure of a magnetotactic spirillum. J Bacteriol, 141(3):1399-1408
    Bazylinski D A, Frankel R B. 2004. Magnetosome formation in prokaryotes. Nat Rev Microbiol, 2(3):217-230
    Bazylinski D A, Frankel R B, Heywood B R, et al. 1995. Controlled biomineralization of magnetite (Fe3O4) and greigite (Fe3S4) in a magnetotactic bacterium. Appl Environ Microbiol, 61(9):3232-3239
    Bazylinski D A, Frankel R B, Jannasch H W. 1988. Anaerobic magnetite production by a marine, magnetotactic bacterium. Nature, 334(6182):518-519
    Bazylinski D A, Moskowitz B M. 1997. Microbial biomineralization of magnetic iron minerals:microbiology, magnetism and environmental significance. Rev Miner Geochem, 35(1):181-223
    Bellini S. 2009. On a unique behavior of freshwater bacteria. Chin J Oceanol Limnol, 27(1):3-5
    Benzerara K, Menguy N. 2009. Looking for traces of life in minerals. Cr Palevol, 8(7):617-628
    Blakemore R P. 1975. Magnetotactic bacteria. Science, 190(4212):377-379
    Blakemore R P. 1982. Magnetotactic bacteria. Annu Rev Microbiol, 36(1):217-238
    Chen Yiran, Zhang Rui, Du Haijian, et al. 2015. A novel species of ellipsoidal multicellular magnetotactic prokaryotes from Lake Yuehu in China. Environ Microbiol, 17(3):637-647
    Cox B L, Popa R, Bazylinski D A, et al. 2002. Organization and elemental analysis of P-, S-, and Fe-rich inclusions in a population of freshwater magnetococci. Geomicrobiol J, 19(4):387-406
    DeLong E F, Frankel R B, Bazylinski D A. 1993. Multiple evolutionary origins of magnetotaxis in bacteria. Science, 259(5096):803-806
    Esquivel D M S, De Barros H G P. 1986. Motion of magnetotactic microorganisms. J Exp Biol, 121(1):153-163
    Farina M, Esquivel D M S, De Barros H G P L. 1990. Magnetic iron-sulphur crystals from a magnetotactic microorganism. Nature, 343(6255):256-258
    Flies C B, Jonkers H M, de Beer D, et al. 2005a. Diversity and vertical distribution of magnetotactic bacteria along chemical gradients in freshwater microcosms. FEMS Microbiol Ecol, 52(2):185-195
    Flies C B, Peplies J, Schüler D. 2005b. Combined approach for characterization of uncultivated magnetotactic bacteria from various aquatic environments. Appl Environ Microbiol, 71(5):2723-2731
    Frankel R B, Bazylinski D A, Johnson M S, et al. 1997. Magneto-aerotaxis in marine coccoid bacteria. Biophys J, 73(2):994-1000
    Gao Li, Zhang Luhua, Hou Jinzhi, et al. 2013. Decomposition of macroalgal blooms influences phosphorus release from the sediments and implications for coastal restoration in Swan Lake, Shandong, China. Ecol Eng, 60:19-28
    Hanzlik M, Winklhofer M, Petersen N. 2002. Pulsed-field-remanence measurements on individual magnetotactic bacteria. J Magn Magn Mater, 248(2):258-267
    Jogler C, Lin Wei, Meyerdierks A, et al. 2009. Toward cloning of the magnetotactic metagenome:identification of magnetosome island gene clusters in uncultivated magnetotactic bacteria from different aquatic sediments. Appl Environ Microbiol, 75(12):3972-3979
    Kawaguchi R, Burgess J G, Sakaguchi T, et al. 1995. Phylogenetic analysis of a novel sulfate-reducing magnetic bacterium, RS-1, demonstrates its membership of the δ-Proteobacteria. FEMS Microbiol Lett, 126(3):277-282
    Keim C N, Lins U, Farina M. 2001. Elemental analysis of uncultured magnetotactic bacteria exposed to heavy metals. Can J Microbiol, 47(12):1132-1136
    Keim C N, Lins U, Farina M. 2003. Iron oxide and iron sulphide crystals in magnetotactic multicellular aggregates. Acta Microsc, 12:3-4
    Keim C N, Solórzano G, Farina M, et al. 2005. Intracellular inclusions of uncultured magnetotactic bacteria. Int Microbiol, 8(2):111-117
    Kolinko S, Jogler C, Katzmann E, et al. 2012. Single-cell analysis reveals a novel uncultivated magnetotactic bacterium within the candidate division OP3. Environ Microbiol, 14(7):1709-1721
    Kolinko S, Richter M, Glöckner F O, et al. 2016. Single-cell genomics of uncultivated deep-branching magnetotactic bacteria reveals a conserved set of magnetosome genes. Environ Microbiol, 18(1):21-37
    Kumar S, Nei M, Dudley J, et al. 2008. MEGA:A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform, 9(4):299-306
    Lefèvre C T, Bernadac A, Yuzhang K, et al. 2009. Isolation and characterization of a magnetotactic bacterial culture from the Mediterranean Sea. Environ Microbiol, 11(7):1646-1657
    Lefèvre C T, Frankel R B, Abreu F, et al. 2011a. Culture-independent characterization of a novel, uncultivated magnetotactic member of the Nitrospirae phylum. Environ Microbiol, 13(2):538-549
    Lefèvre C T, Frankel R B, Pósfai M, et al. 2011b. Isolation of obligately alkaliphilic magnetotactic bacteria from extremely alkaline environments. Environ Microbiol, 13(8):2342-2350
    Lefèvre C T, Menguy N, Abreu F, et al. 2011c. A cultured greigite-producing magnetotactic bacterium in a novel group of sulfate-reducing bacteria. Science, 334(6063):1720-1723
    Lefèvre C T, Viloria N, Schmidt M L, et al. 2012. Novel magnetite-producing magnetotactic bacteria belonging to the Gammaproteobacteria. ISME J, 6(2):440-450
    Lefèvre C T, Wu Longfei. 2013. Evolution of the bacterial organelle responsible for magnetotaxis. Trends Microbiol, 21(10):534-543
    Lin Wei, Bazylinski D A, Xiao Tian, et al. 2014a. Life with compass:diversity and biogeography of magnetotactic bacteria. Environ Microbiol, 16(9):2646-2658
    Lin Wei, Deng Aihua, Wang Zhang, et al. 2014b. Genomic insights into the uncultured genus ‘Candidatus Magnetobacterium’ in the phylum Nitrospirae. ISME J, 8(12):2463-2477
    Lin Wei, Li Jinhua, Pan Yongxin. 2012. Newly isolated but uncultivated magnetotactic bacterium of the phylum Nitrospirae from Beijing, China. Appl Environ Microbiol, 78(3):668-675
    Lin Wei, Li Jinhua, Schüler D, et al. 2009. Diversity analysis of magnetotactic bacteria in Lake Miyun, northern China, by restriction fragment length polymorphism. Syst Appl Microbiol, 32(5):342-350
    Lin Wei, Pan Yongxin. 2009. Uncultivated magnetotactic cocci from Yuandadu Park in Beijing, China. Appl Environ Microbiol, 75(12):4046-4052
    Lins U, Farina M. 1999. Phosphorus-rich granules in uncultured magnetotactic bacteria. FEMS Microbiol Lett, 172(1):23-28
    Lins U, Freitas F, Keim C N, et al. 2003. Simple homemade apparatus for harvesting uncultured magnetotactic microorganisms. Braz J Microbiol, 34(2):111-116
    Mann S, Sparks N H C, Board R G. 1990. Magnetotactic bacteria:microbiology, biomineralization, palaeomagnetism and biotechnology. Adv Microb Physiol, 31:125-181
    Maratea D, Blakemore R P. 1981. Aquaspirillum magnetotacticum sp. nov., a Magnetic Spirillum. Int J Syst Bacteriol, 31(4):452-455
    Matsunaga T, Sakaguchi T, Tadokoro F. 1991. Magnetite formation by a magnetic bacterium capable of growing aerobically. Appl Microbiol Biotechnol, 35(5):651-655
    Meldrum F C, Mann S, Heywood B R, et al. 1993. Electron microscopy study of magnetosomes in a cultured coccoid magnetotactic bacterium. Proc Roy Soc B Biol Sci, 251(1332):231-236
    Pan Hongmiao, Zhu Kailing, Song Tao, et al. 2008. Characterization of a homogeneous taxonomic group of marine magnetotactic cocci within a low tide zone in the China Sea. Environ Microbiol, 10(5):1158-1164
    Sakaguchi T, Arakaki A, Matsunaga T. 2002. Desulfovibrio magneticus sp. nov., a novel sulfate-reducing bacterium that produces intracellular single-domain-sized magnetite particles. Int J Syst Evol Microbiol, 52(1):215-221
    Schüler D. 1999. Formation of magnetosomes in magnetotactic bacteria. J Mol Microbiol Biotechnol, 1(1):79-86
    Schüler D. 2002. The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense. Int Microbiol, 5(4):209-214
    Silva K T, Abreu F, Keim C N, et al. 2008. Ultrastructure and cytochemistry of lipid granules in the many-celled magnetotactic prokaryote, ‘Candidatus Magnetoglobus multicellularis’. Micron, 39(8):1387-1392
    Simmons S L, Sievert S M, Frankel R B, et al. 2004. Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Appl Environ Microbiol, 70(10):6230-6239
    Spring S, Amann R, Ludwig W, et al. 1992. Phylogenetic diversity and identification of nonculturable magnetotactic bacteria. Syst Appl Microbiol, 15(1):116-122
    Spring S, Amann R, Ludwig W, et al. 1993. Dominating role of an unusual magnetotactic bacterium in the microaerobic zone of a freshwater sediment. Appl Environ Microbiol, 59(8):2397-2403
    Spring S, Bazylinski D A. 2006. Magnetotactic bacteria. In:Dworkin M, Falkow S, Rosenberg E, et al., eds. The Prokaryotes. New York:Springer, 2:842-862
    Spring S, Lins U, Amann R, et al. 1998. Phylogenetic affiliation and ultrastructure of uncultured magnetic bacteria with unusually large magnetosomes. Arch Microbiol, 169(2):136-147
    Spring S, Schleifer K H. 1995. Diversity of magnetotactic bacteria. Syst Appl Microbiol, 18(2):147-153
    Stolz J F, Chang S B R, Kirschvink J L. 1989. Biogenic magnetite in stromatolites:I. Occurrence in modern sedimentary environments. Precambrian Res, 43(4):295-304
    Tamura K, Dudley J, Nei M, et al. 2007. MEGA4:molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol, 24(8):1596-1599
    Thompson J D, Higgins D G, Gibson T J. 1994. CLUSTAL W:improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res, 22(22):4673-4680
    Vali H, Forster O, Amarantidis G, et al. 1987. Magnetotactic bacteria and their magnetofossils in sediments. Earth and Planetary Science Letters, 86(2-4):389-400
    Wang Yinzhao, Lin Wei, Li Jinhua, et al. 2015. Characterizing and optimizing magnetosome production of Magnetospirillum sp. XM-1 isolated from Xi'an City Moat, China. FEMS Microbiol Lett, 362(21):1-8, doi: 10.1093/femsle/fnv167[DOI:10.1093/femsle/fnv167]
    Wenter R, Wanner G, Schüler D, et al. 2009. Ultrastructure, tactic behaviour and potential for sulfate reduction of a novel multicellular magnetotactic prokaryote from North Sea sediments. Environ Microbiol, 11(6):1493-1505
    Wolfe R S, Thauer R K, Pfennig N. 1987. A ‘capillary racetrack’ method for isolation of magnetotactic bacteria. FEMS Microbiol Lett, 45(1):31-35
    Xing Su'e, Pan Hongmiao, Zhu Kailing, et al. 2008. Diversity of marine magnetotactic bacteria in the Huiquan bay near Qingdao city. High Technol Lett (in Chinese), 18(3):312-317
    Xu Cong, Zhang Wenyan, Chen Yiran, et al. 2016. Diversity of magnetotactic bacteria in the intertidal zone of Taiping Bay, Qingdao. Acta Ecol Sinica, 36(14):4346-4354, doi: 10.5846/stxb201412012380[DOI:10.5846/stxb201412012380]
    Zhang Rui, Chen Yiran, Du Haijian, et al. 2014. Characterization and phylogenetic identification of a species of spherical multicellular magnetotactic prokaryotes that produces both magnetite and greigite crystals. Res Microbiol, 165 (7):481-489
    Zhou Ke, Pan Hongmiao, Zhang Shengda, et al. 2011. Occurrence and microscopic analyses of multicellular magnetotactic prokaryotes from coastal sediments in the Yellow Sea. Chin J Oceanol Limnol, 29(2):246-251
    Zhou Ke, Zhang Wenyan, Pan Hongmiao, et al. 2013. Adaptation of spherical multicellular magnetotactic prokaryotes to the geochemically variable habitat of an intertidal zone. Environ Microbiol, 15(5):1595-1605
    Zhou Ke, Zhang Wenyan, Yuzhang K, et al. 2012. A novel genus of multicellular magnetotactic prokaryotes from the Yellow Sea. Environ Microbiol, 14(2):405-413
    Zhu Kailing, Pan Hongmiao, Li Jinhua, et al. 2010. Isolation and characterization of a marine magnetotactic spirillum axenic culture QH-2 from an intertidal zone of the China Sea. Res Microbiol, 161(4):276-283
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (1114) PDF downloads(1292) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return