Swarming motility

Fraser, Gillian M.; Hughes, Colin

doi:10.1016/s1369-5274(99)00033-8

Cited by 268 publications

(312 citation statements)

References 57 publications

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“…subtilis swarmers move over swarm plates in a thin fluid film, and show coordinated movement of swirling and streaming packs Swarmers in P. mirabilis are long filamentous cells and are abundantly flagellated (Fraser & Hughes, 1999), while their equivalents in E. coli and Salmonella (McCarter, 2010) are much less elongated, with only a moderate increase in flagella. Similarly, for B. subtilis on LB plates, cells at the swarm front are not filamentous (Kearns & Losick, 2003;Julkowska et al, 2005).…”

Section: Resultsmentioning

confidence: 99%

Single-cell analysis in situ in a Bacillus subtilis swarming community identifies distinct spatially separated subpopulations differentially expressing hag (flagellin), including specialized swarmers

et al. 2011

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Single-cell analysis in situ in a Bacillus subtilis swarming community identifies distinct spatially separated subpopulations differentially expressing hag (flagellin), including specialized swarmers The non-domesticated Bacillus subtilis strain 3610 displays, over a wide range of humidity, hyperbranched, dendritic, swarming-like migration on a minimal agar medium. At high (70 %) humidity, the laboratory strain 168 sfp + (producing surfactin) behaves very similarly, although this strain carries a frameshift mutation in swrA, which another group has shown under their conditions (which include low humidity) is essential for swarming. We reconcile these different results by demonstrating that, while swrA is essential for dendritic migration at low humidity (30-40 %), it is dispensable at high humidity. Dendritic migration (flagella-and surfactin-dependent) of strains 168 sfp + swrA and 3610 involves elongation of dendrites for several hours as a monolayer of cells in a thin fluid film. This enabled us to determine in situ the spatiotemporal pattern of expression of some key players in migration as dendrites develop, using gfp transcriptional fusions for hag (encoding flagellin), comA (regulation of surfactin synthesis) as well as eps (exopolysaccharide synthesis). Quantitative (singlecell) analysis of hag expression in situ revealed three spatially separated subpopulations or cell types: (i) networks of chains arising early in the mother colony (MC), expressing eps but not hag; (ii) largely immobile cells in dendrite stems expressing intermediate levels of hag; and (iii) a subpopulation of cells with several distinctive features, including very low comA expression but hyper-expression of hag (and flagella). These specialized cells emerge from the MC to spearhead the terminal 1 mm of dendrite tips as swirling and streaming packs, a major characteristic of swarming migration. We discuss a model for this swarming process, emphasizing the importance of population density and of the complementary roles of packs of swarmers driving dendrite extension, while non-mobile cells in the stems extend dendrites by multiplication. INTRODUCTIONThe formation of bacterial communities, such as Bacillus subtilis colonies, was shown recently, while this work was in progress, to occur through a developmental-like program, associated with the presence of different cell types (see Vlamakis et al., 2008;Lemon et al., 2008;Ló pez & Kolter, 2010). Another form of community swarming migration over a surface, apparently occurring in thin fluid films, requires flagella, a surfactant and the production of specialized swarmer cells ( , 2008). Two types of swarming-like migration by B. subtilis have been described. On Luria broth (LB) agar at low humidity and 37 u C (primarily analysed with nondomesticated strains such as 3610), migration proceeds as an expanding confluent field, headed by small groups of bacteria, apparently with little change in individual size (Kearns & Losick, 2003;Julkowska et al., 2004). In contrast, we have described the...

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Section: Resultsmentioning

confidence: 99%

Single-cell analysis in situ in a Bacillus subtilis swarming community identifies distinct spatially separated subpopulations differentially expressing hag (flagellin), including specialized swarmers

et al. 2011

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“…Such a mode of motility allows bacteria to escape local stresses, translocate to a better nutritional environment and efficiently invade host tissue (Fraser and Hughes, 1999;Rashid and Kornberg, 2000;Harshey, 2003). However, despite the benefits, for many bacterial species the ability to migrate on solid surfaces does not exist or is dependent on high surface wetness and thus, restricted to specific environmental conditions (Wang et al, 2005;Kearns, 2010).…”

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Surface-motility induction, attraction and hitchhiking between bacterial species promote dispersal on solid surfaces

et al. 2013

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The ability to move on solid surfaces provides ecological advantages for bacteria, yet many bacterial species lack this trait. We found that Xanthomonas spp. overcome this limitation by making use of proficient motile bacteria in their vicinity. Using X. perforans and Paenibacillus vortex as models, we show that X. perforans induces surface motility, attracts proficient motile bacteria and 'rides' them for dispersal. In addition, X. perforans was able to restore surface motility of strains that lost this mode of motility under multiple growth cycles in the lab. The described interaction occurred both on agar plates and tomato leaves and was observed between several xanthomonads and motile bacterial species. Thus, suggesting that this motility induction and hitchhiking strategy might be widespread and ecologically important. This study provides an example as to how bacteria can rely on the abilities of their neighboring species for their own benefit, signifying the importance of a communal organization for fitness.

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“…This process and other forms of surface motility (reviewed in ref. 9) are found in many bacterial genera (11)(12)(13)(14)(15). Swarmer cells are often hyperflagellated, elongated, and multinucleated.…”

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“…It has been suggested that glycolipid and͞or lipopeptide biosurfactants thereby produced function as wetting agents (16). The migration front is preceded by a visible layer of slime-like extracellular material as observed, for example, for Burkholderia cepacia (12,17). Within the matrix of extracellular polymeric material, the population densities are obviously extremely high (17).…”

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confidence: 99%

Quorum signal molecules as biosurfactants affecting swarming in Rhizobium etli

Daniels

Reynaert

Hoekstra

et al. 2006

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

139

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Swarming motility is suggested to be a social phenomenon that enables groups of bacteria to coordinately and rapidly move atop solid surfaces. This multicellular behavior, during which the apparently organized bacterial populations are embedded in an extracellular slime layer, has previously been linked with biofilm formation and virulence. Many population density-controlled activities involve the activation of complex signaling pathways using small diffusible molecules, also known as autoinducers. In Gramnegative bacteria, quorum sensing (QS) is achieved primarily by means of N-acylhomoserine lactones (AHLs). Here, we report on a dual function of AHL molecules in controlling swarming behavior of Rhizobium etli, the bacterial symbiotic partner of the common bean plant. The major swarming regulator of R. etli is the cinIR QS system, which is specifically activated in swarming cells by its cognate AHL and other long-chain AHLs. This signaling role of long-chain AHLs is required for high-level expression of the cin and rai QS systems. Besides this signaling function, the long-chain AHLs also have a direct role in surface movement of swarmer cells as these molecules possess significant surface activity and induce liquid flows, known as Marangoni flows, as a result of gradients in surface tension at biologically relevant concentrations. These results point to an as-yet-undisclosed direct role of long-chain AHL molecules as biosurfactants.cell-cell signaling ͉ motility ͉ quorum sensing

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Swarming motility

Cited by 268 publications

References 57 publications

Single-cell analysis in situ in a Bacillus subtilis swarming community identifies distinct spatially separated subpopulations differentially expressing hag (flagellin), including specialized swarmers

Single-cell analysis in situ in a Bacillus subtilis swarming community identifies distinct spatially separated subpopulations differentially expressing hag (flagellin), including specialized swarmers

Surface-motility induction, attraction and hitchhiking between bacterial species promote dispersal on solid surfaces

Quorum signal molecules as biosurfactants affecting swarming in Rhizobium etli

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