{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,19]],"date-time":"2026-10-19T12:48:07Z","timestamp":1792414087537,"version":"4.4.0"},"reference-count":48,"publisher":"American Society for Microbiology","issue":"2","license":[{"start":{"date-parts":[[2009,1,15]],"date-time":"2009-01-15T00:00:00Z","timestamp":1231977600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["J Bacteriol"],"published-print":{"date-parts":[[2009,1,15]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n          <jats:p>\n            Electron cryotomography was used to analyze the structure of the Lyme disease spirochete,\n            <jats:italic>Borrelia burgdorferi<\/jats:italic>\n            . This methodology offers a new means for studying the native architecture of bacteria by eliminating the chemical fixing, dehydration, and staining steps of conventional electron microscopy. Using electron cryotomography, we noted that membrane blebs formed at the ends of the cells. These blebs may be precursors to vesicles that are released from cells grown in vivo and in vitro. We found that the periplasmic space of\n            <jats:italic>B. burgdorferi<\/jats:italic>\n            was quite narrow (16.0 nm) compared to those of\n            <jats:italic>Escherichia coli<\/jats:italic>\n            and\n            <jats:italic>Pseudomonas aeruginosa<\/jats:italic>\n            . However, in the vicinity of the periplasmic flagella, this space was considerably wider (42.3 nm). In contrast to previous results, the periplasmic flagella did not form a bundle but rather formed a tight-fitting ribbon that wraps around the protoplasmic cell cylinder in a right-handed sense. We show how the ribbon configuration of the assembled periplasmic flagella is more advantageous than a bundle for both swimming and forming the flat-wave morphology. Previous results indicate that\n            <jats:italic>B. burgdorferi<\/jats:italic>\n            motility is dependent on the rotation of the periplasmic flagella in generating backward-moving waves along the length of the cell. This swimming requires that the rotation of the flagella exerts force on the cell cylinder. Accordingly, a ribbon is more beneficial than a bundle, as this configuration allows each periplasmic flagellum to have direct contact with the cell cylinder in order to exert that force, and it minimizes interference between the rotating filaments.\n          <\/jats:p>","DOI":"10.1128\/jb.01288-08","type":"journal-article","created":{"date-parts":[[2008,11,15]],"date-time":"2008-11-15T01:44:43Z","timestamp":1226713483000},"page":"600-607","update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":84,"title":["The Flat-Ribbon Configuration of the Periplasmic Flagella of\n            <i>Borrelia burgdorferi<\/i>\n            and Its Relationship to Motility and Morphology"],"prefix":"10.1128","volume":"191","author":[{"given":"Nyles W.","family":"Charon","sequence":"first","affiliation":[{"name":"Department of Microbiology, Immunology and Cell Biology, Robert C. Byrd Health Sciences Center, West Virginia University, Morgantown, West Virginia 26506-9177"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stuart F.","family":"Goldstein","sequence":"additional","affiliation":[{"name":"Department of Genetics, Cell Biology, and Development, 6-160 Jackson Hall, University of Minnesota, Minneapolis, Minnesota 55455"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Marko","sequence":"additional","affiliation":[{"name":"Resource for Visualization of Biological Complexity, Wadsworth Center, Empire State Plaza, Albany, New York 12201-0509"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chyongere","family":"Hsieh","sequence":"additional","affiliation":[{"name":"Resource for Visualization of Biological Complexity, Wadsworth Center, Empire State Plaza, Albany, New York 12201-0509"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linda L.","family":"Gebhardt","sequence":"additional","affiliation":[{"name":"New York State Department of Health, Wadsworth Center, David Axelrod Institute, 120 New Scotland Avenue, Albany, New York 12208"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M. Abdul","family":"Motaleb","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology and Cell Biology, Robert C. Byrd Health Sciences Center, West Virginia University, Morgantown, West Virginia 26506-9177"},{"name":"Department of Microbiology and Immunology, Brody School of Medicine, East Carolina University, Greenville, North Carolina 27834"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charles W.","family":"Wolgemuth","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, University of Connecticut Health Center, Farmington, Connecticut 06030-3505"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ronald J.","family":"Limberger","sequence":"additional","affiliation":[{"name":"New York State Department of Health, Wadsworth Center, David Axelrod Institute, 120 New Scotland Avenue, Albany, New York 12208"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nancy","family":"Rowe","sequence":"additional","affiliation":[{"name":"Supercomputer Institute, 599 Walter Library, University of Minnesota, Minneapolis, Minnesota 55455"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_2_2_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.01913-06"},{"key":"e_1_3_2_3_2","doi-asserted-by":"publisher","DOI":"10.1128\/mr.50.4.381-400.1986"},{"key":"e_1_3_2_4_2","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/0006-291X(90)91734-A","volume":"167","year":"1990","unstructured":"Beck, G., J. L. Benach, and G. S. Habicht. 1990. Isolation, preliminary chemical characterization, and biological activity of Borrelia burgdorferi peptidoglycan. Biochem. Biophys. Res. Commun. 167 : 89-95.","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"e_1_3_2_5_2","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/S0022-5193(76)80074-4","volume":"56","year":"1976","unstructured":"Berg, H. C. 1976. How spirochetes may swim. J. Theor. Biol. 56 : 269-273.","journal-title":"J. Theor. Biol."},{"key":"e_1_3_2_6_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.181.16.4725-4733.1999"},{"key":"e_1_3_2_7_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.182.9.2445-2452.2000"},{"key":"e_1_3_2_8_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.184.1.1-17.2002"},{"key":"e_1_3_2_9_2","first-page":"38","year":"1984","unstructured":"Canale-Parola, E. 1984. The spirochetes, p. 38-70. In N. R. Krieg and J. G. Holt (ed.), Bergey's manual of systematic bacteriology. Williams and Wilkins, Baltimore, MD.","journal-title":"Bergey's manual of systematic bacteriology"},{"key":"e_1_3_2_10_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.137.3.1413-1416.1979"},{"key":"e_1_3_2_11_2","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1146\/annurev.genet.36.041602.134359","volume":"36","year":"2002","unstructured":"Charon, N. W., and S. F. Goldstein. 2002. Genetics of motility and chemotaxis of a fascinating group of bacteria: the spirochetes. Annu. Rev. Genet. 36 : 47-73.","journal-title":"Annu. Rev. Genet."},{"key":"e_1_3_2_12_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.174.3.832-840.1992"},{"key":"e_1_3_2_13_2","doi-asserted-by":"publisher","DOI":"10.1128\/jcm.29.6.1162-1170.1991"},{"key":"e_1_3_2_14_2","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1017\/S0033583500004297","volume":"21","year":"1988","unstructured":"Dubochet, J., M. Adrian, J. J. Chang, J. C. Homo, J. Lepault, A. W. McDowall, and P. Schultz. 1988. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21 : 129-228.","journal-title":"Q. Rev. Biophys."},{"key":"e_1_3_2_15_2","unstructured":"Electron energy-loss spectroscopy in the electron microscope. 1986"},{"key":"e_1_3_2_16_2","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1006\/jsbi.1996.0030","volume":"116","year":"1996","unstructured":"Frank, J., M. Radermacher, P. Penczek, J. Zhu, Y. Li, M. Ladjadj, and A. Leith. 1996. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116 : 190-199.","journal-title":"J. Struct. Biol."},{"key":"e_1_3_2_17_2","doi-asserted-by":"publisher","DOI":"10.1038\/37551"},{"key":"e_1_3_2_18_2","first-page":"109","volume":"3","year":"1989","unstructured":"Garon, C. F., D. W. Dorward, and M. D. Corwin. 1989. Structural features of Borrelia burgdorferi\u2014the Lyme disease spirochete: silver staining for nucleic acids. Scanning Microsc. Suppl. 3 : 109-115.","journal-title":"Scanning Microsc. Suppl."},{"key":"e_1_3_2_19_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.178.22.6539-6545.1996"},{"key":"e_1_3_2_20_2","doi-asserted-by":"crossref","first-page":"3433","DOI":"10.1073\/pnas.91.8.3433","volume":"91","year":"1994","unstructured":"Goldstein, S. F., N. W. Charon, and J. A. Kreiling. 1994. Borrelia burgdorferi swims with a planar waveform similar to that of eukaryotic flagella. Proc. Natl. Acad. Sci. USA 91 : 3433-3437.","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"e_1_3_2_21_2","first-page":"543","volume":"57","year":"1984","unstructured":"Hovind-Hougen, K. 1984. Ultrastructure of spirochetes isolated from Ixodes ricinus and Ixodes dammini. Yale J. Biol. Med. 57 : 543-548.","journal-title":"Yale J. Biol. Med."},{"key":"e_1_3_2_22_2","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.jsb.2008.03.009","volume":"163","year":"2008","unstructured":"Izard, J., C. E. Hsieh, R. J. Limberger, C. A. Mannella, and M. Marko. 2008. Native cellular architecture of Treponema denticola revealed by cryo-electron tomography. J. Struct. Biol. 163 : 10-17.","journal-title":"J. Struct. Biol."},{"key":"e_1_3_2_23_2","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/j.sbi.2007.03.002","volume":"17","year":"2007","unstructured":"Jensen, G. J., and A. Briegel. 2007. How electron cryotomography is opening a new window onto prokaryotic ultrastructure. Curr. Opin. Struct. Biol. 17 : 260-267.","journal-title":"Curr. Opin. Struct. Biol."},{"key":"e_1_3_2_24_2","doi-asserted-by":"crossref","first-page":"1205","DOI":"10.1093\/infdis\/162.5.1205","volume":"162","year":"1990","unstructured":"Kimsey, R. B., and A. Spielman. 1990. Motility of Lyme disease spirochetes in fluids as viscous as the extracellular matrix. J. Infect. Dis. 162 : 1205-1208.","journal-title":"J. Infect. Dis."},{"key":"e_1_3_2_25_2","doi-asserted-by":"crossref","first-page":"6169","DOI":"10.1073\/pnas.092010499","volume":"99","year":"2002","unstructured":"Li, C., R. G. Bakker, M. A. Motaleb, M. L. Sartakova, F. C. Cabello, and N. W. Charon. 2002. Asymmetrical flagellar rotation in Borrelia burgdorferi nonchemotactic mutants. Proc. Natl. Acad. Sci. USA 99 : 6169-6174.","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"e_1_3_2_26_2","first-page":"345","volume":"2","year":"2000","unstructured":"Li, C., M. A. Motaleb, M. Sal, S. F. Goldstein, and N. W. Charon. 2000. Spirochete periplasmic flagella and motility. J. Mol. Microbiol. Biotechnol. 2 : 345-354.","journal-title":"J. Mol. Microbiol. Biotechnol."},{"key":"e_1_3_2_27_2","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1159\/000077867","volume":"7","year":"2004","unstructured":"Limberger, R. J. 2004. The periplasmic flagellum of spirochetes. J. Mol. Microbiol. Biotechnol. 7 : 30-40.","journal-title":"J. Mol. Microbiol. Biotechnol."},{"key":"e_1_3_2_28_2","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1111\/j.1365-2958.2006.05272.x","volume":"61","year":"2006","unstructured":"Mashburn-Warren, L. M., and M. Whiteley. 2006. Special delivery: vesicle trafficking in prokaryotes. Mol. Microbiol. 61 : 839-846.","journal-title":"Mol. Microbiol."},{"key":"e_1_3_2_29_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.185.20.6112-6118.2003"},{"key":"e_1_3_2_30_2","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/S1047-8477(02)00020-5","volume":"138","year":"2002","unstructured":"McEwen, B. F., M. Marko, C. E. Hsieh, and C. Mannella. 2002. Use of frozen-hydrated axonemes to assess imaging parameters and resolution limits in cryoelectron tomography. J. Struct. Biol. 138 : 47-57.","journal-title":"J. Struct. Biol."},{"key":"e_1_3_2_31_2","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1146\/annurev.biochem.77.061206.173846","volume":"77","year":"2008","unstructured":"Morris, D. M., and G. J. Jensen. 2008. Toward a biomechanical understanding of whole bacterial cells. Annu. Rev. Biochem. 77 : 583-613.","journal-title":"Annu. Rev. Biochem."},{"key":"e_1_3_2_32_2","doi-asserted-by":"crossref","first-page":"10899","DOI":"10.1073\/pnas.200221797","volume":"97","year":"2000","unstructured":"Motaleb, M. A., L. Corum, J. L. Bono, A. F. Elias, P. Rosa, D. S. Samuels, and N. W. Charon. 2000. Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions. Proc. Natl. Acad. Sci. USA 97 : 10899-10904.","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"e_1_3_2_33_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.187.23.7963-7969.2005"},{"key":"e_1_3_2_34_2","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1038\/nature05015","volume":"442","year":"2006","unstructured":"Murphy, G. E., J. R. Leadbetter, and G. J. Jensen. 2006. In situ structure of the complete Treponema primitia flagellar motor. Nature 442 : 1062-1064.","journal-title":"Nature"},{"key":"e_1_3_2_35_2","doi-asserted-by":"crossref","first-page":"1184","DOI":"10.1111\/j.1365-2958.2008.06120.x","volume":"67","year":"2008","unstructured":"Murphy, G. E., E. G. Matson, J. R. Leadbetter, H. C. Berg, and G. J. Jensen. 2008. Novel ultrastructures of Treponema primitia and their implications for motility. Mol. Microbiol. 67 : 1184-1195.","journal-title":"Mol. Microbiol."},{"key":"e_1_3_2_36_2","first-page":"341","volume":"2","year":"2000","unstructured":"Paster, B. J., and F. E. Dewhirst. 2000. Phylogenetic foundation of spirochetes. J. Mol. Microbiol. Biotechnol. 2 : 341-344.","journal-title":"J. Mol. Microbiol. Biotechnol."},{"key":"e_1_3_2_37_2","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1016\/0304-3991(95)00078-X","volume":"60","year":"1995","unstructured":"Penczek, P., M. Marko, K. Buttle, and J. Frank. 1995. Double-tilt electron tomography. Ultramicroscopy 60 : 393-410.","journal-title":"Ultramicroscopy"},{"key":"e_1_3_2_38_2","first-page":"132","volume":"1","year":"1980","unstructured":"Radermacher, M., and W. Hoppe. 1980. Properties of 3-D reconstructions from projections from conical tilting compared to single-axis tilting, p. 132-133. In P. Brederoo and G. Boom (ed.), Proceedings of the 7th European Congress on Electron Microscopy, vol. 1. Seventh European Congress on Electron Microscopy Foundation, Leiden, The Netherlands.","journal-title":"Properties of 3-D reconstructions from projections from conical tilting compared to single-axis tilting"},{"key":"e_1_3_2_39_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.176.1.21-31.1994"},{"key":"e_1_3_2_40_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.179.5.1628-1635.1997"},{"key":"e_1_3_2_41_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.01421-07"},{"key":"e_1_3_2_42_2","doi-asserted-by":"crossref","first-page":"4850","DOI":"10.1073\/pnas.080068797","volume":"97","year":"2000","unstructured":"Sartakova, M., E. Dobrikova, and F. C. Cabello. 2000. Development of an extrachromosomal cloning vector system for use in Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA 97 : 4850-4855.","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"e_1_3_2_43_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.183.22.6558-6564.2001"},{"key":"e_1_3_2_44_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.00257-06"},{"key":"e_1_3_2_45_2","doi-asserted-by":"publisher","DOI":"10.1128\/iai.61.9.3892-3900.1993"},{"key":"e_1_3_2_46_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.182.10.2793-2801.2000"},{"key":"e_1_3_2_47_2","doi-asserted-by":"crossref","first-page":"1181","DOI":"10.1111\/j.1365-2958.2008.06111.x","volume":"67","year":"2008","unstructured":"Wolgemuth, C., S. F. Goldstein, and N. W. Charon. 2008. Electron cryotomography reveals novel structures of a recently cultured termite gut spirochete. Mol. Microbiol. 67 : 1181-1183.","journal-title":"Mol. Microbiol."},{"key":"e_1_3_2_48_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1086\/313899","volume":"31","year":"2000","unstructured":"Wormser, G. P., R. B. Nadelman, R. J. Dattwyler, D. T. Dennis, E. D. Shapiro, A. C. Steere, T. J. Rush, D. W. Rahn, P. K. Coyle, D. H. Persing, D. Fish, and B. J. Luft. 2000. Practice guidelines for the treatment of Lyme disease. Clin. Infect. Dis. 31(Suppl. 1): 1-14.","journal-title":"Clin. Infect. Dis."},{"key":"e_1_3_2_49_2","doi-asserted-by":"crossref","first-page":"3777","DOI":"10.1073\/pnas.0610106104","volume":"104","year":"2007","unstructured":"Zhang, P., C. M. Khursigara, L. M. Hartnell, and S. Subramaniam. 2007. Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy. Proc. Natl. Acad. Sci. USA 104 : 3777-3781.","journal-title":"Proc. Natl. Acad. Sci. USA"}],"container-title":["Journal of Bacteriology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/JB.01288-08","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/JB.01288-08","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,7,29]],"date-time":"2021-07-29T17:09:42Z","timestamp":1627578582000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/JB.01288-08"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,1,15]]},"references-count":48,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2009,1,15]]}},"alternative-id":["10.1128\/JB.01288-08"],"URL":"https:\/\/doi.org\/10.1128\/jb.01288-08","relation":{},"ISSN":["0021-9193","1098-5530"],"issn-type":[{"value":"0021-9193","type":"print"},{"value":"1098-5530","type":"electronic"}],"subject":[],"published":{"date-parts":[[2009,1,15]]},"assertion":[{"value":"2008-09-14","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2008-10-31","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2020-12-20","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}