Skip to main content
Log in

Characterization of dominant giant rod-shaped magnetotactic bacteria from a low tide zone of the China Sea

Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

Magnetotactic bacteria are a group of Gram-negative bacteria that synthesize magnetic crystals, enabling them to navigate in relation to magnetic field lines. Morphologies of magnetotactic bacteria include spirillum, coccoid, rod, vibrio, and multicellular morphotypes. The coccid shape is generally the most abundant morphotype among magnetotactic bacteria. Here we describe a species of giant rod-shaped magnetotactic bacteria (designated QR-1) collected from sediment in the low tide zone of Huiquan Bay (Yellow Sea, China). This morphotype accounted for 90% of the magnetotactic bacteria collected, and the only taxonomic group which was detected in the sampling site. Microscopy analysis revealed that QR-1 cells averaged (6.71±1.03)×(1.54±0.20) μm in size, and contained in each cell 42–146 magnetosomes that are arranged in a bundle formed one to four chains along the long axis of the cell. The QR-1 cells displayed axial magnetotaxis with an average velocity of 70±28 μm/s. Transmission electron microscopy based analysis showed that QR-1 cells had two tufts of flagella at each end. Phylogenetic analysis of the 16S rRNA genes revealed that QR-1 together with three other rod-shaped uncultivated magnetotactic bacteria are clustered into a deep branch of Alphaproteobacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  • Abreu F, Silva K T, Leão P, Guedes I A, Keim C N, Farina M, Lins U. 2013. Cell adhesion, multicellular morphology, and magnetosome distribution in the multicellular magnetotactic prokaryote Candidatus Magnetoglobus multicellularis. Microsc. Microanal., 19 (3): 535–543.

    Article  Google Scholar 

  • Achbergerová L, Nahálka J. 2011. Polyphosphate-an ancient energy source and active metabolic regulator. Microb. Cell. Fact., 10 (1): 63.

    Article  Google Scholar 

  • Amann R I, Krumholz L, Stahl D A. 1990. Fluorescentoligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J. Bacteriol., 172 (2): 762–770.

    Article  Google Scholar 

  • Atsumi T, Maekawa Y, Yamada T, Kawagishi I, Imae Y, Homma M. 1996. Effect of viscosity on swimming by the lateral and polar flagella of Vibrio alginolyticus. J. Bacteriol., 178 (16): 5 024–5 026.

    Article  Google Scholar 

  • Balkwill D L, Maratea D, Blakemore R P. 1980. Ultrastructure of a magnetotactic spirillum. J. Bacteriol., 141 (3): 1 399–1 408.

    Google Scholar 

  • Bazylinski D A, Frankel R B. 2004. Magnetosome formation in prokaryotes. Nat. Rev. Microbiol., 2 (3): 217–230.

    Article  Google Scholar 

  • Bazylinski D A, Williams T J, Lefèvre C T, Berg R J, Zhang C L, Bowser S S, Dean A J, Beveridge T J. 2013. Magnetococcus marinus gen. nov., sp. nov., a marine, magnetotactic bacterium that represents a novel lineage (Magnetococcaceae fam. nov., Magnetococcales ord. nov.) at the base of the Alphaproteobacteria. Int. J. Syst. Evol. Microbiol., 63 (3): 801–808.

    Article  Google Scholar 

  • Chen Y R, Zhang R, Du H J, Pan H M, Zhang W Y, Zhou K, Li J H, Xiao T, Wu L F. 2015. A novel species of ellipsoidal multicellular magnetotactic prokaryotes from Lake Yuehu in China. Environ. Microbiol., 17 (3): 637–647.

    Article  Google Scholar 

  • Chen Y R, Zhang W Y, Zhou K, Pan H M, Du H J, Xu C, Xu J H, Pradel N, Santini C L, Li J H, Huang H, Pan Y X, Xiao T, Wu L F. 2016. Novel species and expanded distribution of ellipsoidal multicellular magnetotactic prokaryotes. Environ. Microbiol. Rep., 8 (2): 218–226.

    Article  Google Scholar 

  • DeLong E F, Frankel R B, Bazylinski D A. 1993. Multiple evolutionary origins of magnetotaxis in bacteria. Science, 259 (5096): 803–806.

    Article  Google Scholar 

  • Faivre D, Schüler D. 2008. Magnetotactic bacteria and magnetosomes. Chem. Rev., 108 (11): 4 875–4 898.

    Article  Google Scholar 

  • Flies C B, Peplies J, Schüler D. 2005. Combined approach for characterization of uncultivated magnetotactic bacteria from various aquatic environments. Appl. Environ. Microbiol., 71 (5): 2 723–2 731.

    Article  Google Scholar 

  • Frankel R B, Bazylinski D A, Johnson M S, Taylor B L. 1997. Magneto-aerotaxis in marine coccoid bacteria. Biophys. J., 73 (2): 994–1 000.

    Article  Google Scholar 

  • Frickmann H, Zautner A E, Moter A, Kikhney J, Hagen R M, Stender H, Poppert S. 2017. Fluorescence in situ hybridization (FISH) in the microbiological diagnostic routine laboratory: a review. Crit. Rev. Microbiol., 43 (3): 263–293.

    Article  Google Scholar 

  • Henrichsen J. 1972. Bacterial surface translocation: a survey and a classification. Bacteriol. Rev., 36 (4): 478–503.

    Google Scholar 

  • Ji B Y, Zhang S D, Zhang W J, Rouy Z, Alberto F, Santini C L, Mangenot S, Gagnot S, Philippe N, Pradel N, Zhang L C, Tempel S, Li Y, Médigue C, Henrissat B, Coutinho P M, Barbe V, Talla E, Wu L F. 2017. The chimeric nature of the genomes of marine magnetotactic coccoid-ovoid bacteria defines a novel group of Proteobacteria. Environ. Microbiol., 19 (3): 1 103–1 119, https://doi.org/10.1111/1462-2920.13637.

    Article  Google Scholar 

  • Jogler C, Wanner G, Kolinko S, Niebler M, Amann R, Petersen N, Kube M, Reinhardt R, Schüler D. 2011. Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branching Nitrospira phylum. Proc. Natl. Acad. Sci. USA, 108 (3): 1 134–1 139.

    Article  Google Scholar 

  • Kearns D B. 2010. A field guide to bacterial swarming motility. Nat. Rev. Microbiol., 8 (9): 634–644.

    Article  Google Scholar 

  • Kolinko S, Jogler C, Katzmann E, Wanner G, Peplies J, Schüler D. 2012. Single-cell analysis reveals a novel uncultivated magnetotactic bacterium within the candidate division OP3. Environ. Microbiol., 14 (7): 1 709–1 721.

    Article  Google Scholar 

  • Kolinko S, Wanner G, Katzmann E, Kiemer F, Fuchs B M, Schüler D. 2013. Clone libraries and single cell genome amplification reveal extended diversity of uncultivated magnetotactic bacteria from marine and freshwater environments. Environ. Microbiol., 15 (5): 1 290–1 301.

    Article  Google Scholar 

  • Kulaev I S, Vagabov V M. 1983. Polyphosphate metabolism in micro-organisms. Adv Microb Physiol, 24: 24–83.

    Google Scholar 

  • Laflamme M, Xiao S H, Kowalewski M. 2009. Osmotrophy in modular Ediacara organisms. Proc. Natl. Acad. Sci. USA, 106 (34): 14 438–14 443.

    Article  Google Scholar 

  • Le Sage D, Arai K, Glenn D R, DeVience S J, Pham L M, Rahn-Lee L, Lukin M D, Yacoby A, Komeili A, Walsworth R L. 2013. Optical magnetic imaging of living cells. Nature, 496 (7446): 486–489.

    Article  Google Scholar 

  • Lefèvre C T, Abreu F, Schmidt M L, Lins U, Frankel R B, Hedlund B P, Bazylinski D A. 2010. Moderately thermophilic magnetotactic bacteria from hot springs in Nevada. Appl. Environ. Microbiol., 76 (11): 3 740–3 743.

    Article  Google Scholar 

  • Lefèvre C T, Bazylinski D A. 2013. Ecology, diversity, and evolution of magnetotactic bacteria. Microbiol. Mol. Biol. R ev., 77 (3): 497–526.

    Article  Google Scholar 

  • Lefèvre C T, Bernadac A, Kui Y Z, Pradel N, Wu L F. 2009. Isolation and characterization of a magnetotactic bacterial culture from the Mediterranean Sea. Environ. Microbiol., 11 (7): 1 646–1 657.

    Article  Google Scholar 

  • Lefèvre C T, Frankel R B, Abreu F, Lins U, Bazylinski D A. 2011. Culture-independent characterization of a novel, uncultivated magnetotactic member of the Nitrospirae phylum. Environ. Microbiol., 13 (2): 538–549.

    Article  Google Scholar 

  • Lefèvre C T, Schmidt M L, Viloria N, Trubitsyn D, Schüler D, Bazylinski D A. 2012. Insight into the evolution of magnetotaxis in Magnetospirillum spp., based on mam gene phylogeny. Appl. Environ. Microbiol., 78 (20): 7 238–7 248.

    Article  Google Scholar 

  • Lefèvre C T, Wu L F. 2013. Evolution of the bacterial organelle responsible for magnetotaxis. Trends Microbiol., 21 (10): 534–543.

    Article  Google Scholar 

  • Lin W, Bazylinski D A, Xiao T, Wu L F, Pan Y X. 2014. Life with compass: diversity and biogeography of magnetotactic bacteria. Environ. Microbiol., 16 (9): 2 646–2 658.

    Article  Google Scholar 

  • Lin W, Li J H, Pan Y X. 2012. Newly isolated but uncultivated magnetotactic bacterium of the phylum Nitrospirae from Beijing, China. Appl. Environ. Microbiol., 78 (3): 668–675.

    Article  Google Scholar 

  • Lin W, Li J H, Schüler D, Jogler C, Pan Y X. 2009. Diversity analysis of magnetotactic bacteria in Lake Miyun, northern China, by restriction fragment length polymorphism. Syst. Appl. Microbiol., 32 (5): 342–350.

    Article  Google Scholar 

  • Lin W, Pan Y X. 2009. Uncultivated magnetotactic cocci from yuandadu park in beijing, China. Appl. Environ. Microbiol., 75 (12): 4 046–4 052.

    Article  Google Scholar 

  • Lin W, Pan Y X. 2015. A putative greigite-type magnetosome gene cluster from the candidate phylum Latescibacteria. Environ. Microbiol. Rep., 7 (2): 237–242.

    Article  Google Scholar 

  • Lin W, Wang Y Z, Gorby Y, Nealson K, Pan Y X. 2013. Integrating niche-based process and spatial process in biogeography of magnetotactic bacteria. Sci. Rep., 3 (1): 1643.

    Article  Google Scholar 

  • Mann S, Sparks N H C, Board R G. 1990. Magnetotactic bacteria: microbiology, biomineralization, palaeomagnetism and biotechnology. Adv. Microb. Physiol., 31: 31–125.

    Google Scholar 

  • Mao X, Liu X. 2015. An initial study of the influences of oxygen conditions on wild-type magnetotactic bacteria in sediment. Chin. Sci. Bull., 60 (1): 88–96. (in Chinese with English abstract)

    Article  Google Scholar 

  • Matsunaga T, Sakaguchi T, Tadokoro F. 1991. Magnetite formation by a magnetic bacterium capable of growing aerobically. Appl. Microbiol. Biotechnol., 35 (5): 651–655.

    Article  Google Scholar 

  • Moench T T, Konetzka W A. 1978. A novel method for the isolation and study of a magnetotactic bacterium. Arch. Microbiol., 119 (2): 203–212.

    Article  Google Scholar 

  • Nan B Y, Zusman D R. 2016. Novel mechanisms power bacterial gliding motility. Mol. Microbiol., 101 (2): 186–193.

    Article  Google Scholar 

  • Pan H M, Zhu K L, Song T, Yu-Zhang K, Lefèvre C, Xing S, Liu M, Zhao S J, Xiao T, Wu L F. 2008. Characterization of a homogeneous taxonomic group of marine magnetotactic cocci within a low tide zone in the China Sea. Environ. Microbiol., 10 (5): 1 158–1 164.

    Article  Google Scholar 

  • Rodrigue S, Malmstrom R R, Berlin A M, Birren B W, Henn M R, Chisholm S W. 2009. Whole genome amplification and de novo assembly of single bacterial cells. PLoS One, 4 (9): e6864.

    Article  Google Scholar 

  • Schaechter M, Maaløe O, Kjeldgaard N O. 1958. Dependency on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. J. Gen. Microbiol., 19 (3): 592–606.

    Article  Google Scholar 

  • Schüler D. 1999. Formation of magnetosomes in magnetotactic bacteria. J. Mol. Microbiol. Biotechnol., 1 (1): 79–86.

    Google Scholar 

  • Schüler D. 2002. The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense. Int. Microbiol., 5 (4): 209–214.

    Article  Google Scholar 

  • Schüler D. 2008. Genetics and cell biology of magnetosome formation in magnetotactic bacteria. FEMS Mic robiol. Rev., 32 (4): 654–672.

    Article  Google Scholar 

  • Schulz H N, Jørgensen B B. 2001. Big bacteria. Annu. Rev. Microbiol., 55 (1): 105–137.

    Article  Google Scholar 

  • Schulz H N, Schulz H D. 2005. Large sulfur bacteria and the formation of phosphorite. Science, 307 (5708): 416–418.

    Article  Google Scholar 

  • Silva K T, Abreu F, Almeida F P, Keim C N, Farina M, Lins U. 2007. Flagellar apparatus of south-seeking many-celled magnetotactic prokaryotes. Microsc. Res. Tech., 70 (1): 10–17.

    Article  Google Scholar 

  • Spormann A M, Wolfe R S. 1984. Chemotactic, magnetotactic and tactile behaviour in a magnetic spirillum. FEMS Microbiol. Lett., 22 (3): 171–177.

    Article  Google Scholar 

  • Spring S, Amann R, Ludwig W, Schleifer K H, Petersen N. 1992. Phylogenetic diversity and identification of nonculturable magnetotactic bacteria. Sy st. Appl. Microbiol., 15 (1): 116–122.

    Article  Google Scholar 

  • Spring S, Amann R, Ludwig W, Schleifer K H, Schüler D, Poralla K, Petersen N. 1995. Phylogenetic analysis of uncultured magnetotactic bacteria from the alpha-subclass of Proteobacteria. Syst. Appl. Microbiol., 17 (4): 501–508.

    Article  Google Scholar 

  • Spring S, Amann R, Ludwig W, Schleifer K H, van Gemerden H, Petersen N. 1993. Dominating role of an unusual magnetotactic bacterium in the microaerobic zone of a freshwater sediment. Appl. Environ. Microbiol., 59 (8): 2 397–2 403.

    Google Scholar 

  • Spring S, Lins U, Amann R, Schleifer K H, Ferreira L C S, Esquivel D M S, Farina M. 1998. Phylogenetic affiliation and ultrastructure of uncultured magnetic bacteria with unusually large magnetosomes. Arch. Microbiol., 169 (2): 136–147.

    Article  Google Scholar 

  • Steinberger R E, Allen A R, Hansa H G, Holden P A. 2002. Elongation correlates with nutrient deprivation in pseudomonas aeruginosa-unsaturates biofilms. Microb. Ecol., 43 (4): 416–423.

    Article  Google Scholar 

  • Taheri-Araghi S, Bradde S, Sauls J T, Hill N S, Levin P A, Paulsson J, Vergassola M, Jun S. 2015. Cell-size control and homeostasis in bacteria. Curr. Biol., 25 (3): 385–391.

    Article  Google Scholar 

  • Taylor B L. 1983. How do bacteria find the optimal concentration of oxygen? Trends Biochem. Sci., 8 (12): 438–441.

    Google Scholar 

  • Turner L, Zhang R J, Darnton N C, Berg H C. 2010. Visualization of flagella during bacterial swarming. J. Bacteriol., 192 (13): 3 259–3 267.

    Article  Google Scholar 

  • Wadhams G H, Armitage J P. 2004. Making sense of it all: bacterial chemotaxis. Nat. Rev. Mol. Cell Biol., 5 (12): 1 024–1 037.

    Article  Google Scholar 

  • Williams T J, Lefèvre C T, Zhao W D, Beveridge T J, Bazylinski D A. 2012. Magnetospira thiophila gen. nov., sp. nov., a marine magnetotactic bacterium that represents a novel lineage within the Rhodospirillaceae (Alphaproteobacteria). Int. J. Syst. Evol. Microbiol., 62 (10): 2 443–2 450.

    Article  Google Scholar 

  • Woyke T, Tighe D, Mavromatis K, Clum A, Copeland A, Schackwitz W, Lapidus A, Wu D Y, McCutcheon J P, McDonald B R, Moran N A, Bristow J, Cheng J F. 2010. One bacterial cell, one complete genome. PLoS One, 5 (4): e10314.

    Article  Google Scholar 

  • Xing S E, Pan H M, Zhu K L, Xiao T, Wu L F. 2008. Diversity of marine magnetotactic bacteria in the Huiquan bay near Qingdao city. Chin. High Technol. Lett., 18 (3): 312–317. (in Chinese with English abstract)

    Google Scholar 

  • Zhang W J, Li Y, Wu L F. 2014. Complex composition and exquisite architecture of bacterial flagellar propellers. Chin. Sci. Bull., 59 (20): 1 912–1 918. (in Chinese with English abstract)

    Article  Google Scholar 

  • Zhang W Y, Zhang S D, Xiao T, Pan Y X, Wu L F. 2010. Geographical distribution of magnetotactic bacteria. Environ. Sci., 31 (2): 450–458. (in Chinese with English abstract)

    Google Scholar 

  • Zhang W Y, Zhou K, Pan H M, Du H J, Chen Y R, Zhang R, Ye W N, Lu C J, Xiao T, Wu L F. 2013. Novel rod-shaped magnetotactic bacteria belonging to the class Alphaproteobacteria. Appl. Environ. Microbiol., 79 (9): 3 137–3 140.

    Article  Google Scholar 

  • Zhang W Y, Zhou K, Pan H M, Yue H D, Jiang M, Xiao T, Wu L F. 2012. Two genera of magnetococci with bean-like morphology from intertidal sediments of the Yellow Sea, China. Appl. Environ. Microbiol., 78 (16): 5 606–5 611.

    Article  Google Scholar 

  • Zhang X H. 2016. Marine Microbiology. 2 nd edn. Science Press, Beijing, China. p.10-11. (in Chinese)

    Google Scholar 

  • Zhou K, Pan H M, Yue H D, Xiao T, Wu LF. 2010. Architecture of flagellar apparatus of marine magnetotactic cocci from Qingdao. Mar. Sci., 34 (12): 88–92. (in Chinese with English abstract)

    Google Scholar 

  • Zhou K, Zhang W Y, Pan H M, Li J H, Yue H D, Xiao T, Wu L F. 2013. Adaptation of spherical multicellular magnetotactic prokaryotes to the geochemically variable habitat of an intertidal zone. Environ. Microbiol., 15 (5): 1 595–1 605.

    Article  Google Scholar 

  • Zhou K, Zhang W Y, Yu-Zhang K, Pan H M, Zhang S D, Zhang W J, Yue H D, Li Y, Xiao T, Wu L F. 2012. A novel genus of multicellular magnetotactic prokaryotes from the Yellow Sea. Environ. Microbiol., 14 (2): 405–413.

    Article  Google Scholar 

  • Zhu K L, Pan H M, Li J H, Yu-Zhang K, Zhang S D, Zhang W Y, Zhou K, Yue H D, Pan Y X, Xiao T, Wu L F. 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.

    Article  Google Scholar 

Download references

Acknowledgement

We thank XU Jianhong for his assistance with biological sampling, JIANG Ming, LIU Jing, and MA Xicheng for their assistance with the TEM analysis, and LIU Wei for supporting our SEM observations.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wenyan Zhang  (张文燕).

Additional information

Supported by the National Natural Science Foundation of China (Nos. 41330962, 41276170) and the National Natural Science Foundation of China—Shandong Joint Fund for Marine Science Research Centers (No. U1606404)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Teng, Z., Zhang, W., Chen, Y. et al. Characterization of dominant giant rod-shaped magnetotactic bacteria from a low tide zone of the China Sea. J. Ocean. Limnol. 36, 783–794 (2018). https://doi.org/10.1007/s00343-018-7072-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-018-7072-2

Keyword

Navigation