Advertisement

Journal of Oceanology and Limnology

, Volume 36, Issue 3, pp 783–794 | Cite as

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

  • Zhaojie Teng (滕兆洁)
  • Wenyan Zhang (张文燕)
  • Yiran Chen (陈一然)
  • Hongmiao Pan (潘红苗)
  • Tian Xiao (肖天)
  • Long-Fei Wu (吴龙飞)
Article
First Online:

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.

Keyword

Alphaproteobacteria flagella motility rod-shaped magnetotactic bacteria 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

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.

References

  1. 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.CrossRefGoogle Scholar
  2. Achbergerová L, Nahálka J. 2011. Polyphosphate-an ancient energy source and active metabolic regulator. Microb. Cell. Fact., 10 (1): 63.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. Balkwill D L, Maratea D, Blakemore R P. 1980. Ultrastructure of a magnetotactic spirillum. J. Bacteriol., 141 (3): 1 399–1 408.Google Scholar
  6. Bazylinski D A, Frankel R B. 2004. Magnetosome formation in prokaryotes. Nat. Rev. Microbiol., 2 (3): 217–230.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. DeLong E F, Frankel R B, Bazylinski D A. 1993. Multiple evolutionary origins of magnetotaxis in bacteria. Science, 259 (5096): 803–806.CrossRefGoogle Scholar
  11. Faivre D, Schüler D. 2008. Magnetotactic bacteria and magnetosomes. Chem. Rev., 108 (11): 4 875–4 898.CrossRefGoogle Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. Henrichsen J. 1972. Bacterial surface translocation: a survey and a classification. Bacteriol. Rev., 36 (4): 478–503.Google Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. Kearns D B. 2010. A field guide to bacterial swarming motility. Nat. Rev. Microbiol., 8 (9): 634–644.CrossRefGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. Kulaev I S, Vagabov V M. 1983. Polyphosphate metabolism in micro-organisms. Adv Microb Physiol, 24: 24–83.Google Scholar
  22. Laflamme M, Xiao S H, Kowalewski M. 2009. Osmotrophy in modular Ediacara organisms. Proc. Natl. Acad. Sci. USA, 106 (34): 14 438–14 443.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. Lefèvre C T, Bazylinski D A. 2013. Ecology, diversity, and evolution of magnetotactic bacteria. Microbiol. Mol. Biol. R ev., 77 (3): 497–526.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. Lefèvre C T, Wu L F. 2013. Evolution of the bacterial organelle responsible for magnetotaxis. Trends Microbiol., 21 (10): 534–543.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. Lin W, Pan Y X. 2009. Uncultivated magnetotactic cocci from yuandadu park in beijing, China. Appl. Environ. Microbiol., 75 (12): 4 046–4 052.CrossRefGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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
  37. 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)CrossRefGoogle Scholar
  38. Matsunaga T, Sakaguchi T, Tadokoro F. 1991. Magnetite formation by a magnetic bacterium capable of growing aerobically. Appl. Microbiol. Biotechnol., 35 (5): 651–655.CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. Nan B Y, Zusman D R. 2016. Novel mechanisms power bacterial gliding motility. Mol. Microbiol., 101 (2): 186–193.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. Schüler D. 1999. Formation of magnetosomes in magnetotactic bacteria. J. Mol. Microbiol. Biotechnol., 1 (1): 79–86.Google Scholar
  45. Schüler D. 2002. The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense. Int. Microbiol., 5 (4): 209–214.CrossRefGoogle Scholar
  46. Schüler D. 2008. Genetics and cell biology of magnetosome formation in magnetotactic bacteria. FEMS Mic robiol. Rev., 32 (4): 654–672.CrossRefGoogle Scholar
  47. Schulz H N, Jørgensen B B. 2001. Big bacteria. Annu. Rev. Microbiol., 55 (1): 105–137.CrossRefGoogle Scholar
  48. Schulz H N, Schulz H D. 2005. Large sulfur bacteria and the formation of phosphorite. Science, 307 (5708): 416–418.CrossRefGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. Spormann A M, Wolfe R S. 1984. Chemotactic, magnetotactic and tactile behaviour in a magnetic spirillum. FEMS Microbiol. Lett., 22 (3): 171–177.CrossRefGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. 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
  54. 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.CrossRefGoogle Scholar
  55. 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.CrossRefGoogle Scholar
  56. 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.CrossRefGoogle Scholar
  57. Taylor B L. 1983. How do bacteria find the optimal concentration of oxygen? Trends Biochem. Sci., 8 (12): 438–441.Google Scholar
  58. 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.CrossRefGoogle Scholar
  59. 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.CrossRefGoogle Scholar
  60. 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.CrossRefGoogle Scholar
  61. 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.CrossRefGoogle Scholar
  62. 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
  63. 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)CrossRefGoogle Scholar
  64. 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
  65. 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.CrossRefGoogle Scholar
  66. 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.CrossRefGoogle Scholar
  67. Zhang X H. 2016. Marine Microbiology. 2 nd edn. Science Press, Beijing, China. p.10-11. (in Chinese)Google Scholar
  68. 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
  69. 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.CrossRefGoogle Scholar
  70. 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.CrossRefGoogle Scholar
  71. 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.CrossRefGoogle Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Zhaojie Teng (滕兆洁)
    • 1
    • 2
    • 3
  • Wenyan Zhang (张文燕)
    • 1
    • 3
  • Yiran Chen (陈一然)
    • 1
    • 3
  • Hongmiao Pan (潘红苗)
    • 1
    • 3
  • Tian Xiao (肖天)
    • 1
    • 3
  • Long-Fei Wu (吴龙飞)
    • 4
    • 5
  1. 1.CAS Key Laboratory of Marine Ecology & Environmental Sciences, Institute of OceanologyChinese Academy of SciencesQingdaoChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Laboratory of Marine Ecology and Environmental ScienceQingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  4. 4.Laboratoire de Chimie Bactérienne, UMR7283, Institut de Microbiologie de la MéditerranéeAix-Marseille Université, CNRSMarseilleFrance
  5. 5.Laboratoire International Associé de la Bio-Minéralisation et Nano-Structures, CNRSMarseilleFrance

Personalised recommendations

Cite article

Buy options