Improvement in Motion Efficiency of the Spirochete Brachyspira pilosicoli in Viscous Environments

Nakamura, Shuichi; Adachi, Yoshikazu; Goto, Tomonobu; Magariyama, Yukio

doi:10.1529/biophysj.105.074336

Cited by 59 publications

(60 citation statements)

References 44 publications

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“…Previous studies have characterized selective pressures favoring particular shapes (7,(9)(10)(11): for example, highly viscous environments may select for the helical cell morphologies observed in spirochete bacteria (12). Thus far, these studies have predominantly focused on selective pressures acting at the level of the individual cell.…”

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confidence: 99%

Cell morphology drives spatial patterning in microbial communities

Smith

Davit

Osborne

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

149

138

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The clearest phenotypic characteristic of microbial cells is their shape, but we do not understand how cell shape affects the dense communities, known as biofilms, where many microbes live. Here, we use individual-based modeling to systematically vary cell shape and study its impact in simulated communities. We compete cells with different cell morphologies under a range of conditions and ask how shape affects the patterning and evolutionary fitness of cells within a community. Our models predict that cell shape will strongly influence the fate of a cell lineage: we describe a mechanism through which coccal (round) cells rise to the upper surface of a community, leading to a strong spatial structuring that can be critical for fitness. We test our predictions experimentally using strains of Escherichia coli that grow at a similar rate but differ in cell shape due to single amino acid changes in the actin homolog MreB. As predicted by our model, cell types strongly sort by shape, with round cells at the top of the colony and rod cells dominating the basal surface and edges. Our work suggests that cell morphology has a strong impact within microbial communities and may offer new ways to engineer the structure of synthetic communities.biofilms | cell morphology | biophysics | self-organization | synthetic biology S ingle-celled microorganisms such as bacteria display significant morphological diversity, ranging from the simple to the complex and exotic (1-3). Phylogenetic studies indicate that particular morphologies have evolved independently multiple times, suggesting that the myriad shapes of modern bacteria may be adaptations to particular environments (4-6). Microbes can also actively change their morphology in response to environmental stimuli, such as changes to nutrient levels or predation (7,8). However, understanding when and why particular cell shapes offer a competitive edge remains an unresolved question in microbiology.Previous studies have characterized selective pressures favoring particular shapes (7, 9-11): for example, highly viscous environments may select for the helical cell morphologies observed in spirochete bacteria (12). Thus far, these studies have predominantly focused on selective pressures acting at the level of the individual cell. However, many species live in dense, surfaceassociated communities known as biofilms, which are fundamental to the biology of microbes and how they affect us-playing major roles in the human microbiome, chronic diseases, antibiotic resistance, biofouling, and waste-water treatment (13-17). As a result, there has been an intensive effort in recent years to understand how the biofilm mode of growth affects microbes and their evolution (18, 19), but we know very little of the importance of cell shape for biofilm biology.In biofilms, microbial cells are often in close physical contact, making mechanical interactions between neighboring cells particularly significant. Recent studies have suggested that rodshaped cells can drive collective behaviors in microbial g...

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mentioning

confidence: 99%

Cell morphology drives spatial patterning in microbial communities

Smith

Davit

Osborne

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

149

138

View full text Add to dashboard Cite

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“…The motility of vegetative bacterial cells increases as the dynamic viscosity of the surrounding fluid increases; above a threshold that varies for different species of bacteria, cell velocity decreases rapidly (17)(18)(19)(20)(21)(22)(23). The viscosity required for complete inhibition of motility varies widely, with values ranging from 0.06 to ϳ1 Pa · s (17).…”

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Flagellum Density Regulates Proteus mirabilis Swarmer Cell Motility in Viscous Environments

et al. 2013

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cProteus mirabilis is an opportunistic pathogen that is frequently associated with urinary tract infections. In the lab, P. mirabilis cells become long and multinucleate and increase their number of flagella as they colonize agar surfaces during swarming. Swarming has been implicated in pathogenesis; however, it is unclear how energetically costly changes in P. mirabilis cell morphology translate into an advantage for adapting to environmental changes. We investigated two morphological changes that occur during swarming-increases in cell length and flagellum density-and discovered that an increase in the surface density of flagella enabled cells to translate rapidly through fluids of increasing viscosity; in contrast, cell length had a small effect on motility. We found that swarm cells had a surface density of flagella that was ϳ5 times larger than that of vegetative cells and were motile in fluids with a viscosity that inhibits vegetative cell motility. To test the relationship between flagellum density and velocity, we overexpressed FlhD 4 C 2 , the master regulator of the flagellar operon, in vegetative cells of P. mirabilis and found that increased flagellum density produced an increase in cell velocity. Our results establish a relationship between P. mirabilis flagellum density and cell motility in viscous environments that may be relevant to its adaptation during the infection of mammalian urinary tracts and movement in contact with indwelling catheters. Proteus mirabilis is a Gram-negative rod-shaped gammaproteobacterium that is commonly associated with urinary tract infections (1) and the biofouling of catheters (2-4). P. mirabilis may also be present in the human gut microflora (5) and is correlated with the incidence of colitis (6, 7). Broth-grown vegetative cells of P. mirabilis are characteristically ϳ2 m long and have a peritrichous distribution of ϳ4 to 10 flagella. The flagella form a bundle that performs work on the surrounding fluid and propels cells forward via a mechanism that is similar to the motility system of Escherichia coli (8, 9).Broth-grown vegetative cells of P. mirabilis in contact with the surface of agar gels infused with nutrients change their morphology, become "swarmers," and colonize the surface by coordinating the movement of large groups of cells (i.e., "swarming") (see Fig. 1A). P. mirabilis swarm colonies exhibit a terraced pattern of concentric rings (see Fig. S1 in the supplemental material) (10). These rings are produced by alternating phases of consolidation, during which the colony does not expand and cells are dedifferentiated into a vegetative cell-like morphology, and swarming, during which cells are motile and differentiated (11). Motility occurs predominantly at the swarm front and decreases with increasing distance from the front; cells near the center of the swarm are nonmotile. Swarming has several characteristics, including the following: (i) the inhibition of cell division to produce long (10-to 70-m) multinucleate cells, (ii) an increase in the surface dens...

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“…Thus, spirochetes differ from other bacteria in that the spirochete organelles for motility-the PFs-reside within the periplasmic space. There is a real advantage to being a spirochete, since these organisms can efficiently swim through highly viscous gel-like media which inhibit the motility of most other motile bacterial species (3,8,34).…”

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confidence: 99%

Genetic Analysis of Spirochete Flagellin Proteins and Their Involvement in Motility, Filament Assembly, and Flagellar Morphology

Wolgemuth

Marko

et al. 2008

J Bacteriol

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The filaments of spirochete periplasmic flagella (PFs) have a unique structure and protein composition. In most spirochetes, the PFs consist of a core of at least three related proteins (FlaB1, FlaB2, and FlaB3) and a sheath of FlaA protein. The functions of these filament proteins remain unknown. In this study, we used a multidisciplinary approach to examine the role of these proteins in determining the composition, shape, and stiffness of the PFs and how these proteins impact motility by using the spirochete Brachyspira (formerly Treponema, Serpulina) hyodysenteriae as a genetic model. A series of double mutants lacking combinations of these PF proteins was constructed and analyzed. The results show the following. First, the diameters of PFs are primarily determined by the sheath protein FlaA, and that FlaA can form a sheath in the absence of an intact PF core. Although the sheath is important to the PF structure and motility, it is not essential. Second, the three core proteins play unequal roles in determining PF structure and swimming speed. The functions of the core proteins FlaB1 and FlaB2 overlap such that either one of these proteins is essential for the spirochete to maintain the intact PF structure and for cell motility. Finally, linear elasticity theory indicates that flagellar stiffness directly affects the spirochete's swimming speed.

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Improvement in Motion Efficiency of the Spirochete Brachyspira pilosicoli in Viscous Environments

Cited by 59 publications

References 44 publications

Cell morphology drives spatial patterning in microbial communities

Cell morphology drives spatial patterning in microbial communities

Flagellum Density Regulates Proteus mirabilis Swarmer Cell Motility in Viscous Environments

Genetic Analysis of Spirochete Flagellin Proteins and Their Involvement in Motility, Filament Assembly, and Flagellar Morphology

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