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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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Dragging of two aggregate structures together by supercoiling of an extended fiber in contact with both. The images were taken from film sequence 1. A right-handed fiber attached to the surface of an aggregate structure swept clockwise around the aggregate from its point of attachment. In frame 3 it made contact with a neighboring structure, supercoiled in frames 4 to 6 and drew the neighboring structure to the surface of the initial structure to which it was connected. The two structures later fused together. This sequence illustrates the mechanism by which exclusion zones become established surrounding large structures.
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Figure 4: Dragging of two aggregate structures together by supercoiling of an extended fiber in contact with both. The images were taken from film sequence 1. A right-handed fiber attached to the surface of an aggregate structure swept clockwise around the aggregate from its point of attachment. In frame 3 it made contact with a neighboring structure, supercoiled in frames 4 to 6 and drew the neighboring structure to the surface of the initial structure to which it was connected. The two structures later fused together. This sequence illustrates the mechanism by which exclusion zones become established surrounding large structures.

Mentions: Large and structurally complex macrofibers form ball-like structures rather than elongated ones as a result of supercoiling. Compare the geometry of forms in frames 1 and 16 of Figure 1. The ball-like forms produced by joining of large fibers are much more sedentary than their precursors. Figure 3 illustrates this. 10 large immobile structures are shown. The paths taken by precursor fibers leading to their contact and joining reveal the distances and directions travelled in the formation of each aggregate structure. For example, several of the initial 6 fibers that eventually became the one large ball-form aggregate shown on the upper left of Figure 3 traversed a distance of 5 mm from their initial positions to their final location in the aggregate structure. They moved over this distance either by "walking" over the plastic surface of the petri dish [10] until they met one-another, or by being "dragged" from one location to another as a result of supercoiling [11]. Structures too large to move themselves by walking can still be dragged from one location to another as shown in Figure 4 provided they acquire an extended fiber attached to their surface. In the case shown two structures too large to walk were drawn together by the supercoiling of an extended fiber that bridged between them. To begin with, the extended fiber had one free end capable of rotating as it grew. When rotation of the free end was prevented by contact with the second large ball structure supercoiling was induced. The two structures were then drawn together by the contraction in length that accompanies supercoiling. See Additional file 3 for an overview of the dragging process.


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)

Dragging of two aggregate structures together by supercoiling of an extended fiber in contact with both. The images were taken from film sequence 1. A right-handed fiber attached to the surface of an aggregate structure swept clockwise around the aggregate from its point of attachment. In frame 3 it made contact with a neighboring structure, supercoiled in frames 4 to 6 and drew the neighboring structure to the surface of the initial structure to which it was connected. The two structures later fused together. This sequence illustrates the mechanism by which exclusion zones become established surrounding large structures.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 4: Dragging of two aggregate structures together by supercoiling of an extended fiber in contact with both. The images were taken from film sequence 1. A right-handed fiber attached to the surface of an aggregate structure swept clockwise around the aggregate from its point of attachment. In frame 3 it made contact with a neighboring structure, supercoiled in frames 4 to 6 and drew the neighboring structure to the surface of the initial structure to which it was connected. The two structures later fused together. This sequence illustrates the mechanism by which exclusion zones become established surrounding large structures.
Mentions: Large and structurally complex macrofibers form ball-like structures rather than elongated ones as a result of supercoiling. Compare the geometry of forms in frames 1 and 16 of Figure 1. The ball-like forms produced by joining of large fibers are much more sedentary than their precursors. Figure 3 illustrates this. 10 large immobile structures are shown. The paths taken by precursor fibers leading to their contact and joining reveal the distances and directions travelled in the formation of each aggregate structure. For example, several of the initial 6 fibers that eventually became the one large ball-form aggregate shown on the upper left of Figure 3 traversed a distance of 5 mm from their initial positions to their final location in the aggregate structure. They moved over this distance either by "walking" over the plastic surface of the petri dish [10] until they met one-another, or by being "dragged" from one location to another as a result of supercoiling [11]. Structures too large to move themselves by walking can still be dragged from one location to another as shown in Figure 4 provided they acquire an extended fiber attached to their surface. In the case shown two structures too large to walk were drawn together by the supercoiling of an extended fiber that bridged between them. To begin with, the extended fiber had one free end capable of rotating as it grew. When rotation of the free end was prevented by contact with the second large ball structure supercoiling was induced. The two structures were then drawn together by the contraction in length that accompanies supercoiling. See Additional file 3 for an overview of the dragging process.

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