Abstract
Multicellular magnetotactic prokaryotes (MMPs) are a group of aggregates composed of 7–45 gram-negative cells synthesizing intracellular magnetic crystals. Although they are thought to be globally distributed, MMPs have been observed only in marine environments in America and Europe. Most MMPs share a rosette-like morphology and biomineralize iron sulfide crystals. In the present study, abundant MMPs were observed, with a density of 26 ind./cm3, in the sediments of a coastal lagoon, Lake Yuehu, in the Yellow Sea. Optical microscopy showed that all of them were rosette shaped with a diameter of 5.5±0.8 μm. Transmission electron microscopy revealed that these MMPs were composed of 10–16 ovoid cells and flagellated peritrichously. High-resolution transmission electron microscopy and energy dispersive X-ray analysis indicated that they biomineralized bullet-shaped magnetite crystals in highly organized parallel chains within which the magnetosomes were oriented in the same direction. This is the first report of MMPs from Asia and demonstrates the ubiquitous distribution of MMPs.
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Abreu F, Martins J L, Silveira T S, Keim C N, Lins de Barros H G P, Filho F J G, Lins U. 2007. ’Candidates Magnetoglobus multicellularis’, a multicellular, magnetotactic prokaryote from a hypersaline environment. International Journal of Systematic and Evolutionary Microbiology, 57(6): 1 318–1 322.
Abreu F, Silva K T, Martins J L, Lins U. 2006. Cell viability in magnetotactic multicellular prokaryotes. International Microbiology, 9(4): 267–272.
Bazylinski D A, Garrattreed A J, Abedi A, Frankel R B. 1993. Copper association with iron sulfide magnetosomes in a magnetotactic bacterium. Archives of Microbiology, 160(1): 35–42.
Bazylinski D A, Moskowitz B M. 1997. Microbial biomineralization of magnetic iron minerals: Microbiology, magnetism and environmental significance. Geomicrobiology: Interactions between Microbes and Minerals, 35: 181–223.
de Beer D, Wenzhöfer F, Ferdelman T G., Boehme S E, Huettel M. 2005. Transport and mineralization rates in North Sea sandy intertidal sediments, Sylt-Rømø Basin, Wadden Sea. Limnology and Oceanography, 50(1): 113–127.
Bellini S. 2009a. Further studies on “magnetosensitive bacteria”. Chinese Journal of Oceanology and Limnology, 27(1): 6–12.
Bellini S. 2009b. On a unique behavior of freshwater bacteria. Chinese Journal of Oceanology and Limnology, 27(1): 3–5.
Blakemore R P. 1975. Magnetotactic bacteria. Science, 190(4212): 377–379.
Delong E F, Frankel R B, Bazylinski D A. 1993. Multiple evolutionary origins of magnetotaxis in bacteria. Science, 259(5096): 803–806.
Faivre D, Schüler D. 2008. Magnetotactic bacteria and magnetosomes. Chemical Reviews, 108(11): 4875–4898.
Farina M, Lins de Barros H. 1983. Ultrastructure of a magnetotactic microorganism. Biology of the Cell, 48(1): 85–88.
Farina M, Esquivel D M S, Lins de Barros H G P. 1990. Magnetic iron-sulfur crystals from a magnetotactic microorganism. Nature, 343(6255): 256–258.
Frankel R B. 2009. The discovery of magnetotactic/magnetosensitive bacteria. Chinese Journal of Oceanology and Limnology, 27(1): 1–2.
Frankel R B, Bazylinski D A, Johnson M S, Taylor B L. 1997. Magneto-aerotaxis in marine coccoid bacteria. Biophysical Journal, 73(2): 994–1 000.
Greenberg M, Canter K, Mahler I, Tornheim A. 2005. Observation of magnetoreceptive behavior in a multicellular magnetotactic prokaryote in higher than geomagnetic fields. Biophysical Journal, 88(2): 1 496–1 499.
Keim C, Lopes Martins J, Lins de Barros H, Lins U, Farina M. 2007. Structure, behavior, ecology and diversity of multicellular magnetotactic prokaryotes. In: Schüler D ed. Magnetoreception and Magnetosomes in Bacteria. Springer, Berlin, Heidelberg, Germany, p. 103–132.
Keim C N, Abreu F, Lins U, Lins de Barros H, Farina M. 2004a. Cell organization and ultrastructure of a magnetotactic multicellular organism. Journal of Structural Biology, 145(3): 254–262.
Keim C N, Lins U, Farina M. 2003. Iron oxide and iron sulphide crystals in magnetotactic multicellular aggregates. Acta Microscopica, 12: 3–4.
Keim C N, Martins J L, Abreu F, Rosado A S, Lins de Barros H, Borojevic R, Lins U, Farina M. 2004b. Multicellular life cycle of magnetotactic prokaryotes. FEMS Microbiology Letters, 240(2): 203–208.
Lefèvre C, Bernadac A, Pradel N, Wu L, Yu-Zhang K, Xiao T, Yonnet J P, Lebouc A, Song T, Fukumori Y. 2007. Characterization of Mediterranean magnetotactic bacteria. Journal of Ocean University of China (English Edition), 6(4): 355–359.
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. Systematic and Applied Microbiology, 32(5): 342–350.
Lins de Barros H G, Esquivel D M, Farina M. 1990. Magnetotaxis. Science Progress, 74(295 Pt 3): 347–359.
Lins U, Keim C, Evans F, Farina M, Buseck P. 2007. Magnetite (Fe304) and greigite (Fe3S4) crystals in multicellular magnetotactic prokaryotes. Geomicrobiology Journal, 24(1): 43–50.
Mann S, Sparks N H, Board R G 1990a. Magnetotactic bacteria: Microbiology, biomineralization, palaeomagnetism and biotechnology. Advances in Microbial Physiology, 31: 125–181.
Mann S, Sparks N H C, Frankel R B, Bazylinski D A, Jannasch H W. 1990b. Biomineralization of ferrimagnetic greigite (Fe3S4) and iron pyrite (FeS2) in a magnetotactic bacterium. Nature, 343(6255): 258–261.
Martins J L, Silveira T S, Silva K T, Lins U. 2009. Salinity dependence of the distribution of multicellular magnetotactic prokaryotes in a hypersaline lagoon. International Microbiology, 12(3): 193–201.
Pósfai M, Buseck P, Bazylinski D A, Frankel R B. 1998a. Iron sulfides from magnetotactic bacteria: Structure, composition, and phase transitions. American Mineralogist, 83(11–12): 1469–1481.
Pósfai M, Buseck P R, Bazylinski D A, Frankel R B. 1998b. Reaction sequence of iron sulfide minerals in bacteria and their use as biomarkers. Science, 280: 880–883.
Pan H M, Zhu K L, Song T, Yu-Zhang K, Lefevre 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. Environmental Microbiology, 10(5): 1158–1164.
Perantoni M, Esquivel D M S, Wajnberg E, Acosta-Avalos D, Cernicchiaro G, Lins de Barros G C H. 2009. Magnetic properties of the microorganism Candidatus Magnetoglobus multicellularis. Naturwissenschaften, 96(6): 685–690.
Rodgers F G, Blakemore R P, Blakemore N A, Frankel R B, Bazylinski D A, Maratea D, Rodgers C. 1990. Intercellular structure in a many-celled magnetotactic prokaryote. Archives of Microbiology, 154(1): 18–22.
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. Microscopy Research and Technique, 70(1): 10–17.
Simmons S L, Edwards K J. 2007. Unexpected diversity in populations of the many-celled magnetotactic prokaryote. Environmental Microbiology, 9(1): 206–215.
Simmons S L, Sievert S M, Frankel R B, Bazylinski D A, Edwards K J. 2004. Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Applied and Environmental Microbiology, 70(10): 6230–6 239.
Wenter R, Wanner G, Schüler D, Overmann J. 2009. Ultrastructure, tactic behaviour and potential for sulfate reduction of a novel multicellular magnetotactic prokaryote from North Sea sediments. Environmental Microbiology, 11(6): 1 493–1 505.
Winklhofer M, Abracado L G, Davila A F, Keim C N, Lins de Barros H G P. 2007. Magnetic optimization in a multicellular magnetotactic organism. Biophysical Journal, 92(2): 661–670.
Wolfe R S, Thauer R K, Pfennig N. 1987. A ‘capillary racetrack’ method for isolation of magnetotactic bacteria. FEMS Microbiology Ecology, 45: 31–35.
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Supported by the National Natural Science Foundation of China (Nos. 40906069, 40776094), the Haiwaijiechuxuezhe-Fund of Chinese Academy of Sciences (No. 2006-1-15), and K. C. WONG Education Foundation
ZHOU Ke and PAN Hongmiao contributed equally to this work
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Zhou, K., Pan, H., Zhang, S. et al. Occurrence and microscopic analyses of multicellular magnetotactic prokaryotes from coastal sediments in the Yellow Sea. Chin. J. Ocean. Limnol. 29, 246–251 (2011). https://doi.org/10.1007/s00343-011-0032-8
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DOI: https://doi.org/10.1007/s00343-011-0032-8