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The mechanisms responsible for 2-dimensional pattern formation in bacterial macrofiber populations grown on solid surfaces: fiber joining and the creation of exclusion zones.

Mendelson NH, Morales D, Thwaites JJ - BMC Microbiol. (2002)

Bottom Line: Observed and expected patterns differ significantly.Cell growth geometry governs in an hierarchical way the formation of these patterns using forces associated with twisting and supercoiling to drive motions and the joining of structures together.Joining by entwining, supercoiling or dragging all require cell growth in a multicellular form, and all result in tightly fused aggregate structures.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USA. nhm@u.arizona.edu

ABSTRACT

Background: When Bacillus subtilis is cultured in a complex fluid medium under conditions where cell separation is suppressed, populations of multicellular macrofibers arise that mature into ball-like structures. The final sedentary forms are found distributed in patterns on the floor of the growth chamber although individual cells have no flagellar-driven motility. The nature of the patterns and their mode of formation are described in this communication.

Results: Time-lapse video films reveal that fiber-fiber contact in high density populations of macrofibers resulted in their joining either by entwining or supercoiling. Joining led to the production of aggregate structures that eventually contained all of the fibers located in an initial area. Fibers were brought into contact by convection currents and motions associated with macrofiber self-assembly such as walking, pivoting and supercoiling. Large sedentary aggregate structures cleared surrounding areas of other structures by dragging them into the aggregate using supercoiling of extended fibers to power dragging. The spatial distribution of aggregate structures in 6 mature patterns containing a total of 637 structures was compared to that expected in random theoretical populations of the same size distributed in the same surface area. Observed and expected patterns differ significantly. The distances separating all nearest neighbors from one another in observed populations were also measured. The average distance obtained from 1451 measurements involving 519 structures was 0.73 cm. These spacings were achieved without the use of flagella or other conventional bacterial motility mechanisms. A simple mathematical model based upon joining of all structures within an area defined by the minimum observed distance between structures in populations explains the observed distributions very well.

Conclusions: Bacterial macrofibers are capable of colonizing a solid surface by forming large multicellular aggregate structures that are distributed in unique two-dimensional patterns. Cell growth geometry governs in an hierarchical way the formation of these patterns using forces associated with twisting and supercoiling to drive motions and the joining of structures together. Joining by entwining, supercoiling or dragging all require cell growth in a multicellular form, and all result in tightly fused aggregate structures.

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Butt splice formation of right-handed FJ7 macrofiber fragments. Eight frames from film sequence 2 show spontaneous end to end joining of fragments produced by entwining of cell filaments at their broken ends. Fragments no longer carrying terminal loops were produced by toothpick disruption of a parental fiber. Once joined the two fragments behaved as integrated components of a single fiber in terms of twisting, bending and writhing motions.
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Figure 2: Butt splice formation of right-handed FJ7 macrofiber fragments. Eight frames from film sequence 2 show spontaneous end to end joining of fragments produced by entwining of cell filaments at their broken ends. Fragments no longer carrying terminal loops were produced by toothpick disruption of a parental fiber. Once joined the two fragments behaved as integrated components of a single fiber in terms of twisting, bending and writhing motions.

Mentions: The joining of macrofibers to one another is a growth-dependent process driven by twist and supercoiling. It requires fiber-fiber contact that impedes the free twisting of one or both structures. Depending upon the geometry of the two structures that make contact and whether or not both ends of a given structure are prevented from rotating, contact results in either entwining of the two, or supercoiling that gives rise to a ball-like form consisting of both partners. Figure 2 illustrates the joining of two fiber fragments by the formation of a functional butt splice. The fragments shown are typical of those produced by toothpick transfer of a mature fiber into fresh medium. Individual cell filaments protruding from the ends of both fragment shafts became entwined with one-another. The newly spliced structure behaved as a single mechanical entity in all it's subsequent behavior, including an experimentally induced helix hand inversion during which all the cell filaments in the fiber's shaft unwound then twisted back together in the opposite helix hand. Additional file 2 shows the dynamics of splice formation and helix hand inversion. The maintenance of the splice throughout inversion illustrates that joining by entwining creates a strong linkage between the two entities. Joining by entwining also occurs when intact mature macrofibers with loops at their ends meet [9]. The resulting structures are irregular in diameter along their length reflecting differences in the diameter and/or topology of the two initial partners. Though irregular, joined structures of this sort are nevertheless mechanically sound and capable of continued self-assembly. They progress to mature ball-forms just as clonal fibers grown in isolation do.


The mechanisms responsible for 2-dimensional pattern formation in bacterial macrofiber populations grown on solid surfaces: fiber joining and the creation of exclusion zones.

Mendelson NH, Morales D, Thwaites JJ - BMC Microbiol. (2002)

Butt splice formation of right-handed FJ7 macrofiber fragments. Eight frames from film sequence 2 show spontaneous end to end joining of fragments produced by entwining of cell filaments at their broken ends. Fragments no longer carrying terminal loops were produced by toothpick disruption of a parental fiber. Once joined the two fragments behaved as integrated components of a single fiber in terms of twisting, bending and writhing motions.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC65521&req=5

Figure 2: Butt splice formation of right-handed FJ7 macrofiber fragments. Eight frames from film sequence 2 show spontaneous end to end joining of fragments produced by entwining of cell filaments at their broken ends. Fragments no longer carrying terminal loops were produced by toothpick disruption of a parental fiber. Once joined the two fragments behaved as integrated components of a single fiber in terms of twisting, bending and writhing motions.
Mentions: The joining of macrofibers to one another is a growth-dependent process driven by twist and supercoiling. It requires fiber-fiber contact that impedes the free twisting of one or both structures. Depending upon the geometry of the two structures that make contact and whether or not both ends of a given structure are prevented from rotating, contact results in either entwining of the two, or supercoiling that gives rise to a ball-like form consisting of both partners. Figure 2 illustrates the joining of two fiber fragments by the formation of a functional butt splice. The fragments shown are typical of those produced by toothpick transfer of a mature fiber into fresh medium. Individual cell filaments protruding from the ends of both fragment shafts became entwined with one-another. The newly spliced structure behaved as a single mechanical entity in all it's subsequent behavior, including an experimentally induced helix hand inversion during which all the cell filaments in the fiber's shaft unwound then twisted back together in the opposite helix hand. Additional file 2 shows the dynamics of splice formation and helix hand inversion. The maintenance of the splice throughout inversion illustrates that joining by entwining creates a strong linkage between the two entities. Joining by entwining also occurs when intact mature macrofibers with loops at their ends meet [9]. The resulting structures are irregular in diameter along their length reflecting differences in the diameter and/or topology of the two initial partners. Though irregular, joined structures of this sort are nevertheless mechanically sound and capable of continued self-assembly. They progress to mature ball-forms just as clonal fibers grown in isolation do.

Bottom Line: Observed and expected patterns differ significantly.Cell growth geometry governs in an hierarchical way the formation of these patterns using forces associated with twisting and supercoiling to drive motions and the joining of structures together.Joining by entwining, supercoiling or dragging all require cell growth in a multicellular form, and all result in tightly fused aggregate structures.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USA. nhm@u.arizona.edu

ABSTRACT

Background: When Bacillus subtilis is cultured in a complex fluid medium under conditions where cell separation is suppressed, populations of multicellular macrofibers arise that mature into ball-like structures. The final sedentary forms are found distributed in patterns on the floor of the growth chamber although individual cells have no flagellar-driven motility. The nature of the patterns and their mode of formation are described in this communication.

Results: Time-lapse video films reveal that fiber-fiber contact in high density populations of macrofibers resulted in their joining either by entwining or supercoiling. Joining led to the production of aggregate structures that eventually contained all of the fibers located in an initial area. Fibers were brought into contact by convection currents and motions associated with macrofiber self-assembly such as walking, pivoting and supercoiling. Large sedentary aggregate structures cleared surrounding areas of other structures by dragging them into the aggregate using supercoiling of extended fibers to power dragging. The spatial distribution of aggregate structures in 6 mature patterns containing a total of 637 structures was compared to that expected in random theoretical populations of the same size distributed in the same surface area. Observed and expected patterns differ significantly. The distances separating all nearest neighbors from one another in observed populations were also measured. The average distance obtained from 1451 measurements involving 519 structures was 0.73 cm. These spacings were achieved without the use of flagella or other conventional bacterial motility mechanisms. A simple mathematical model based upon joining of all structures within an area defined by the minimum observed distance between structures in populations explains the observed distributions very well.

Conclusions: Bacterial macrofibers are capable of colonizing a solid surface by forming large multicellular aggregate structures that are distributed in unique two-dimensional patterns. Cell growth geometry governs in an hierarchical way the formation of these patterns using forces associated with twisting and supercoiling to drive motions and the joining of structures together. Joining by entwining, supercoiling or dragging all require cell growth in a multicellular form, and all result in tightly fused aggregate structures.

Show MeSH
Related in: MedlinePlus