The dynamic behavior of bacterial macrofibers growing with one end prevented from rotating: variation in shaft rotation along the fiber's length, and supercoil movement on a solid surface toward the constrained end

Persistent Link:
http://hdl.handle.net/10150/610048
Title:
The dynamic behavior of bacterial macrofibers growing with one end prevented from rotating: variation in shaft rotation along the fiber's length, and supercoil movement on a solid surface toward the constrained end
Author:
Mendelson, Neil; Shipman, Patrick; Roy, Darshan; Chen, Liling; Thwaites, John
Affiliation:
Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USA; Department of Mathematics, University of Arizona, Tucson, AZ 85721, USA; Department of Biochemistry and Molecular Biophysics, University of Arizona, Tucson, AZ 85721, USA; Gonville and Caius College, Cambridge CB2 1TA, U.K
Issue Date:
2003
Publisher:
BioMed Central
Citation:
BMC Microbiology 2003, 3:18 http://www.biomedcentral.com/1471-2180/3/18
Journal:
BMC Microbiology
Rights:
© 2003 Mendelson et al; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose
Collection Information:
This item is part of the UA Faculty Publications collection. For more information this item or other items in the UA Campus Repository, contact the University of Arizona Libraries at repository@u.library.arizona.edu.
Abstract:
BACKGROUND:Bacterial macrofibers twist as they grow, writhe, supercoil and wind up into plectonemic structures (helical forms the individual filaments of which cannot be taken apart without unwinding) that eventually carry loops at both of their ends. Terminal loops rotate about the axis of a fiber's shaft in contrary directions at increasing rate as the shaft elongates. Theory suggests that rotation rates should vary linearly along the length of a fiber ranging from maxima at the loop ends to zero at an intermediate point. Blocking rotation at one end of a fiber should lead to a single gradient: zero at the blocked end to maximum at the free end. We tested this conclusion by measuring directly the rotation at various distances along fiber length from the blocked end. The movement of supercoils over a solid surface was also measured in tethered macrofibers.RESULTS:Macrofibers that hung down from a floating wire inserted through a terminal loop grew vertically and produced small plectonemic structures by supercoiling along their length. Using these as markers for shaft rotation we observed a uniform gradient of initial rotation rates with slopes of 25.6degrees/min. mm. and 36.2degrees/min. mm. in two different fibers. Measurements of the distal tip rotation in a third fiber as a function of length showed increases proportional to increases in length with constant of proportionality 79.2 rad/mm. Another fiber tethered to the floor grew horizontally with a length-doubling time of 74 min, made contact periodically with the floor and supercoiled repeatedly. The supercoils moved over the floor toward the tether at approximately 0.06 mm/min, 4 times faster than the fiber growth rate. Over a period of 800 minutes the fiber grew to 23 mm in length and was entirely retracted back to the tether by a process involving 29 supercoils.CONCLUSIONS:The rate at which growing bacterial macrofibers rotated about the axis of the fiber shaft measured at various locations along fibers in structures prevented from rotating at one end reveal that the rate varied linearly from zero at the blocked end to maximum at the distal end. The increasing number of twisting cells in growing fibers caused the distal end to continuously rotate faster. When the free end was intermittently prevented from rotating a torque developed which was relieved by supercoiling. On a solid surface the supercoils moved toward the end permanently blocked from rotating as a result of supercoil rolling over the surface and the formation of new supercoils that reduced fiber length between the initial supercoil and the wire tether. All of the motions are ramifications of cell growth with twist and the highly ordered multicellular state of macrofibers.
EISSN:
1471-2180
DOI:
10.1186/1471-2180-3-18
Version:
Final published version
Additional Links:
http://www.biomedcentral.com/1471-2180/3/18

Full metadata record

DC FieldValue Language
dc.contributor.authorMendelson, Neilen
dc.contributor.authorShipman, Patricken
dc.contributor.authorRoy, Darshanen
dc.contributor.authorChen, Lilingen
dc.contributor.authorThwaites, Johnen
dc.date.accessioned2016-05-20T08:57:23Z-
dc.date.available2016-05-20T08:57:23Z-
dc.date.issued2003en
dc.identifier.citationBMC Microbiology 2003, 3:18 http://www.biomedcentral.com/1471-2180/3/18en
dc.identifier.doi10.1186/1471-2180-3-18en
dc.identifier.urihttp://hdl.handle.net/10150/610048-
dc.description.abstractBACKGROUND:Bacterial macrofibers twist as they grow, writhe, supercoil and wind up into plectonemic structures (helical forms the individual filaments of which cannot be taken apart without unwinding) that eventually carry loops at both of their ends. Terminal loops rotate about the axis of a fiber's shaft in contrary directions at increasing rate as the shaft elongates. Theory suggests that rotation rates should vary linearly along the length of a fiber ranging from maxima at the loop ends to zero at an intermediate point. Blocking rotation at one end of a fiber should lead to a single gradient: zero at the blocked end to maximum at the free end. We tested this conclusion by measuring directly the rotation at various distances along fiber length from the blocked end. The movement of supercoils over a solid surface was also measured in tethered macrofibers.RESULTS:Macrofibers that hung down from a floating wire inserted through a terminal loop grew vertically and produced small plectonemic structures by supercoiling along their length. Using these as markers for shaft rotation we observed a uniform gradient of initial rotation rates with slopes of 25.6degrees/min. mm. and 36.2degrees/min. mm. in two different fibers. Measurements of the distal tip rotation in a third fiber as a function of length showed increases proportional to increases in length with constant of proportionality 79.2 rad/mm. Another fiber tethered to the floor grew horizontally with a length-doubling time of 74 min, made contact periodically with the floor and supercoiled repeatedly. The supercoils moved over the floor toward the tether at approximately 0.06 mm/min, 4 times faster than the fiber growth rate. Over a period of 800 minutes the fiber grew to 23 mm in length and was entirely retracted back to the tether by a process involving 29 supercoils.CONCLUSIONS:The rate at which growing bacterial macrofibers rotated about the axis of the fiber shaft measured at various locations along fibers in structures prevented from rotating at one end reveal that the rate varied linearly from zero at the blocked end to maximum at the distal end. The increasing number of twisting cells in growing fibers caused the distal end to continuously rotate faster. When the free end was intermittently prevented from rotating a torque developed which was relieved by supercoiling. On a solid surface the supercoils moved toward the end permanently blocked from rotating as a result of supercoil rolling over the surface and the formation of new supercoils that reduced fiber length between the initial supercoil and the wire tether. All of the motions are ramifications of cell growth with twist and the highly ordered multicellular state of macrofibers.en
dc.language.isoenen
dc.publisherBioMed Centralen
dc.relation.urlhttp://www.biomedcentral.com/1471-2180/3/18en
dc.rights© 2003 Mendelson et al; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purposeen
dc.titleThe dynamic behavior of bacterial macrofibers growing with one end prevented from rotating: variation in shaft rotation along the fiber's length, and supercoil movement on a solid surface toward the constrained enden
dc.typeArticleen
dc.identifier.eissn1471-2180en
dc.contributor.departmentDepartment of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USAen
dc.contributor.departmentDepartment of Mathematics, University of Arizona, Tucson, AZ 85721, USAen
dc.contributor.departmentDepartment of Biochemistry and Molecular Biophysics, University of Arizona, Tucson, AZ 85721, USAen
dc.contributor.departmentGonville and Caius College, Cambridge CB2 1TA, U.Ken
dc.identifier.journalBMC Microbiologyen
dc.description.collectioninformationThis item is part of the UA Faculty Publications collection. For more information this item or other items in the UA Campus Repository, contact the University of Arizona Libraries at repository@u.library.arizona.edu.en
dc.eprint.versionFinal published versionen
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