Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-22T11:14:44.878Z Has data issue: false hasContentIssue false

Cell Adhesion, Multicellular Morphology, and Magnetosome Distribution in the Multicellular Magnetotactic Prokaryote Candidatus Magnetoglobus multicellularis

Published online by Cambridge University Press:  03 April 2013

Fernanda Abreu
Affiliation:
Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, 21941-902, Rio de Janeiro, RJ, Brazil
Karen Tavares Silva
Affiliation:
Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, 21941-902, Rio de Janeiro, RJ, Brazil
Pedro Leão
Affiliation:
Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, 21941-902, Rio de Janeiro, RJ, Brazil
Iame Alves Guedes
Affiliation:
Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, 21941-902, Rio de Janeiro, RJ, Brazil
Carolina Neumann Keim
Affiliation:
Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, 21941-902, Rio de Janeiro, RJ, Brazil
Marcos Farina
Affiliation:
Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, 21941-902, Rio de Janeiro, RJ, Brazil
Ulysses Lins*
Affiliation:
Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, 21941-902, Rio de Janeiro, RJ, Brazil
*
*Corresponding author. E-mail: [email protected]
Get access

Abstract

Candidatus Magnetoglobus multicellularis is an uncultured magnetotactic multicellular prokaryote composed of 17-40 Gram-negative cells that are capable of synthesizing organelles known as magnetosomes. The magnetosomes of Ca. M. multicellularis are composed of greigite and are organized in chains that are responsible for the microorganism's orientation along magnetic field lines. The characteristics of the microorganism, including its multicellular life cycle, magnetic field orientation, and swimming behavior, and the lack of viability of individual cells detached from the whole assembly, are considered strong evidence for the existence of a unique multicellular life cycle among prokaryotes. It has been proposed that the position of each cell within the aggregate is fundamental for the maintenance of its distinctive morphology and magnetic field orientation. However, the cellular organization of the whole organism has never been studied in detail. Here, we investigated the magnetosome organization within a cell, its distribution within the microorganism, and the intercellular relationships that might be responsible for maintaining the cells in the proper position within the microorganism, which is essential for determining the magnetic properties of Ca. M. multicellularis during its life cycle. The results indicate that cellular interactions are essential for the determination of individual cell shape and the magnetic properties of the organism and are likely directly associated with the morphological changes that occur during the multicellular life cycle of this species.

Type
Biological Applications
Copyright
Copyright © Microscopy Society of America 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abedin, M. & King, M. (2010). Diverse evolutionary paths to cell adhesion. Trends Cell Biol 20, 434472.CrossRefGoogle ScholarPubMed
Abreu, F., Martins, J.L., Silveira, T.S., Keim, C.N., Lins De Barros, H.G.P., Gueiros-Filho, F. & Lins, U. (2007). Candidatus Magnetoglobus multicellularis,’ a multicellular magnetotactic prokaryote from a hypersaline environment. Int J Syst Evol Microbiol 57, 13181322.Google Scholar
Abreu, F., Silva, K.T., Martins, J.L. & Lins, U. (2006). Cell viability in magnetotactic multicellular prokaryotes. Int Microbiol 9, 267272.Google ScholarPubMed
Acosta-Avalos, D.A., Azevedo, M.L.S., Andrade, T.S. & Lins De Barros, H. (2012). Magnetic configuration model for the multicellular magnetotactic prokaryote Candidatus Magnetoglobus multicellularis. Eur Biophys J 41, 405413.CrossRefGoogle ScholarPubMed
Briegel, A., Ortegac, D.R., Tochevaa, E.I., Wuichetd, K., Lia, Z., Chena, S., Mullere, A., Iancua, C.V., Murphya, G.E., Dobroa, M.J., Zhulind, I.B. & Jensena, G.J. (2009). Universal architecture of bacterial chemoreceptor arrays. PNAS 106, 1718117186.CrossRefGoogle ScholarPubMed
Farina, M., Lins De Barros, H., Esquivel, D.M.S. & Danon, J. (1983). Ultrastructure of a magnetotactic microorganism. Biol Cell 48, 8588.Google Scholar
Grimm, R., Singh, H., Rachel, R., Typke, D., Zillig, W. & Baumeister, W. (1998). Electron tomography of ice-embedded prokaryotic cells. Biophys J 74, 10311042.Google Scholar
Gumbiner, B.M. (1996). Cell adhesion: The molecular basis of tissue architecture and morphogenesis. Cell 84, 345357.CrossRefGoogle ScholarPubMed
Izard, J., Hsieh, C.E., Limberger, R.J., Mannella, C.A. & Marko, M. (2008). Native cellular architecture of Treponema denticola revealed by cryo-electron tomography. J Struct Biol 163, 1017.Google Scholar
Katzmann, E., Müller, F.D., Lang, C., Messerer, M., Winklhofer, M., Plitzko, J.M. & Schüler, D. (2011). Magnetosome chains are recruited to cellular division sites and split by asymmetric septation. Mol Microbiol 82, 13161329.CrossRefGoogle ScholarPubMed
Keim, C.N., Abreu, F., Lins, U., Barros, H.G.L. & Farina, M. (2004a). Cell organization and ultrastructure of a magnetotactic multicellular organism. J Struct Biol 145, 254262.CrossRefGoogle ScholarPubMed
Keim, C.N., Martins, J.L, Abreu, F., Rosado, A.S., Lins De Barros, H.P., Borojevic, R., Lins, U. & Farina, M. (2004b). Multicellular life cycle of magnetotactic prokaryotes. FEMS Microbiol Lett 240, 203208.CrossRefGoogle ScholarPubMed
Keim, C.N., Martins, J.L., Lins de Barros, H., Lins, U. & Farina, M. (2007). Structure, behavior, ecology and diversity of multicellular magnetotactic prokaryotes. In Magnetoreception and Magnetosomes in Bacteria, Schüler, D. (Ed.), pp. 103132. Berlin, Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Kürner, J., Frangakis, A.S. & Baumeister, W. (2005). Cryo-electron tomography reveals the cytoskeletal structure of Spiroplasma melliferum . Science 307, 436438.Google Scholar
Lins, U. & Farina, M. (1999). Organization of cells in magnetotactic multicellular aggregates. Microbiol Res 154, 913.CrossRefGoogle Scholar
Lins, U., Freitas, F., Keim, C.N., Lins De Barros, H.G.P., Esquivel, D.M.S. & Farina, M. (2003). Simple homemade apparatus for harvesting uncultured magnetotactic microorganisms. Braz J Microbiol 34, 111116.Google Scholar
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. Int Microbiol 12, 193201.Google Scholar
Oschman, J.L. & Wall, B.J. (1972). Calcium binding to intestinal membranes. J Cell Biol 55, 5867.Google Scholar
Rodgers, F.G., Blakemore, R.P., Blakemore, N.A., Frankel, R.B., Bazylinski, D.A., Maratea, D. & Rodgers, N. (1990). Intercellular structure in a many-celled magnetotactic prokaryote. Arch Microbiol 154, 1822.Google Scholar
Silva, K.T., Abreu, F., Almeida, F.P., Keim, C.N., Farina, M. & Lins, U. (2007). The flagellar apparatus in south-seeking many-celled magnetotactic prokaryotes. Microsc Res Techn 70, 1017.CrossRefGoogle ScholarPubMed
Spicer, S.S., Hardin, J.H. & Greene, W.B. (1968). Nuclear precipitates in pyroantimonate-osmium tetroxide-fixed tissues. J Cell Biol 39, 216221.CrossRefGoogle ScholarPubMed
Thiéry, J.P. (1967). Mise en evidence des polysaccharides sur coupes fines en microscopieéléctronique. J Microsc 6, 9871018.Google Scholar
Wanner, G., Vogl, K. & Overmann, J. (2008). Ultrastructural characterization of the prokaryotic symbiosis in “Chlorochromatium aggregatum.” J Bacteriol 190, 37213730.CrossRefGoogle ScholarPubMed
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. Environ Microbiol 11, 14931505.Google Scholar
Winklhofer, M., Abraçado, L.G., Davila, A.F., Keim, C.N. & Lins de Barros, H.G.P. (2007). Magnetic optimization in a multicellular magnetotactic organism. Biophys J 92, 661670.CrossRefGoogle Scholar
Young, K.D. (2007). Bacterial morphology: Why have different shapes? Curr Opin Microbiol 10, 596600.CrossRefGoogle ScholarPubMed
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 2, 405413.Google Scholar