Stigmergy co-ordinates multicellular collective behaviours during Myxococcus xanthus surface migration

Gloag, Erin S.; Turnbull, Lynne; Javed, Muhammad Awais; Wang, Huabin; Gee, Michelle L.; Wade, Scott A; Whitchurch, Cynthia B.

doi:10.1038/srep26005

Cited by 31 publications

(32 citation statements)

References 49 publications

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“…Moreover, gliding cells deposit a slime trail. The function and composition of slime are unknown; however, slime may promote the adhesion of cells to the substratum and may contain polysaccharides and OM vesicles (Ducret et al , ; ; Gloag et al , ). We conclude that LPS is (conditionally) important for both motility systems.…”

Section: Discussionmentioning

confidence: 99%

“…Conversely, transfer of lipoproteins may also have negative effects on recipients, as is the case for the transfer of toxins that kill non-immune recipient cells (Vassallo et al, 2017). Other toxins that kill non-immune cells are transferred in a contact-dependent manner by the type VI secretion system (Gong et al, 2018;Troselj et al, 2018). Finally, during the starvation-induced formation of spore-filled fruiting bodies, transmission of the cell-cell contact-dependent C-signal is essential for the completion of this developmental program (Kim and Kaiser, 1990a;1990b).…”

Section: Introductionmentioning

confidence: 99%

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Identification of the lipopolysaccharide O‐antigen biosynthesis priming enzyme and the O‐antigen ligase in Myxococcus xanthus: critical role of LPS O‐antigen in motility and development

Pérez‐Burgos

García‐Romero

Jung

et al. 2019

Molecular Microbiology

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Summary Myxococcus xanthus is a model bacterium to study social behavior. At the cellular level, the different social behaviors of M. xanthus involve extensive cell–cell contacts. Here, we used bioinformatics, genetics, heterologous expression and biochemical experiments to identify and characterize the key enzymes in M. xanthus implicated in O‐antigen and lipopolysaccharide (LPS) biosynthesis and examined the role of LPS O‐antigen in M. xanthus social behaviors. We identified WbaPMx (MXAN_2922) as the polyisoprenyl‐phosphate hexose‐1‐phosphate transferase responsible for priming O‐antigen synthesis. In heterologous expression experiments, WbaPMx complemented a Salmonella enterica mutant lacking the endogenous WbaP that primes O‐antigen synthesis, indicating that WbaPMx transfers galactose‐1‐P to undecaprenyl‐phosphate. We also identified WaaLMx (MXAN_2919), as the O‐antigen ligase that joins O‐antigen to lipid A‐core. Our data also support the previous suggestion that WzmMx (MXAN_4622) and WztMx (MXAN_4623) form the Wzm/Wzt ABC transporter. We show that mutations that block different steps in LPS O‐antigen synthesis can cause pleiotropic phenotypes. Also, using a wbaPMx deletion mutant, we revisited the role of LPS O‐antigen and demonstrate that it is important for gliding motility, conditionally important for type IV pili‐dependent motility and required to complete the developmental program leading to the formation of spore‐filled fruiting bodies.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Identification of the lipopolysaccharide O‐antigen biosynthesis priming enzyme and the O‐antigen ligase in Myxococcus xanthus: critical role of LPS O‐antigen in motility and development

Pérez‐Burgos

García‐Romero

Jung

et al. 2019

Molecular Microbiology

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“…Exopolysaccharides, the major fraction of ECM, form polymeric networks that provide essential structural support and surface adhesion for biofilms (Berk et al ., ). ECM of the soil bacterium Myxococcus xanthus contains EPS (∼55%), proteins (∼45%) and a small amount of lipids and extracellular DNA (Curtis et al ., ; Behmlander and Dworkin, ; Hu et al ., ; Gloag et al ., ). M. xanthus EPS is composed of various monosaccharides including glucose, rhamnose, mannose and N ‐acetyl glucosamine (Behmlander and Dworkin, ; Gibiansky et al ., ).…”

Section: Introductionmentioning

confidence: 97%

“…Third, pili assembly and EPS production are mutually regulated (Yang et al ., ; Li et al ., ). Fourth, M. xanthus cells, like P. aeruginosa , also show trail‐following behaviors (Gibiansky et al ., ; Gloag et al ., ). Fifth, in a recent report, Berleman et al found that EPS forms honeycomb‐like microchannels that facilitate S‐motility and biofilm formation by aligning individual cells (Berleman et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Exopolysaccharides promote Myxococcus xanthus social motility by inhibiting cellular reversals

Zhou

Nan

2016

Molecular Microbiology

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SummaryThe biofilm-forming bacterium Myxococcus xanthus moves on surfaces as structured swarms utilizing type IV pili-dependent social (S) motility. In contrast to isolated cells that reverse their moving direction frequently, individual cells within swarms rarely reverse. The regulatory mechanisms that inhibit cellular reversal and promote the formation of swarms are not well understood. Here we show that exopolysaccharides (EPS), the major extracellular components of M. xanthus swarms, inhibit cellular reversal in a concentration-dependent manner. Thus, individual wild-type cells reverse less frequently in swarms due to high local EPS concentrations. In contrast, cells defective in EPS production hyper-reverse their moving direction and show severe defects in Smotility. Surprisingly, S-motility and wild-type reversal frequency are restored in double mutants that are defective in both EPS production and the Frz chemosensory system, indicating that EPS regulates cellular reversal in parallel to the Frz pathway. Here we clarify that besides functioning as the structural scaffold in biofilms, EPS is a self-produced signal that coordinates the group motion of the social bacterium M. xanthus.

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“…In addition, several bacterial species modify their local environment and cooperative behaviors to promote swarm colony expansion. For example, surface-motile cells appear to migrate along shared tracks comprised of furrows in the medium lined with extracellular material in Pseudomonas aeruginosa and M. xanthus (41)(42)(43). In P. mirabilis, swarm colonies can produce extracellular slime trails that appear to spatially coordinate swarming cells to promote swarm colony expansion (44).…”

Section: Discussionmentioning

confidence: 99%

Swarming bacteria respond to increasing barriers to motility by increasing cell length and modifying colony structure

Little

Austerman

Zheng

et al. 2018

Preprint

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Organisms can alter morphology and behaviors in response to environmental stimuli such as mechanical forces exerted by surface conditions. The bacterium Proteus mirabilis responds to surface-based growth by enhancing cell length and degree of cell-cell interactions. Cells grow as approximately 2-micrometer rigid rods and independently swim in liquid. By contrast on hard agar surfaces, cells elongate up to 40-fold into snake-like cells that move as a collective group across the surface. Here we have elucidated that individual cell size and degree of cell-cell interactions increased across a continuous gradient that correlates with increasing agar density. We further demonstrate that interactions between the lipopolysaccharide (LPS) component of the outer membrane and the immediate local environment modified these responses by reducing agar-associated barriers to motility. Loss of LPS structures corresponded with increased cell elongation on any given surface. These micrometer-scale changes to cell shape and collective interactions corresponded with centimeter-scale changes in the overall visible structure of the swarm colony. It is well-appreciated in eukaryotes that mechanical forces impact cell shape and migration. Here we propose that bacteria can also dynamically respond to the mechanical forces of surface conditions by altering cell shape, individual motility, and collective migration. IntroductionEukaryotic and prokaryotic cells undergo alterations, including changes in cell morphology and collective behaviors, in response to interactions with the physical environment. For example, robust swarmers such as the human pathogens Proteus mirabilis and Vibrio parahaemolyticus (1) can swim as short, rigid rod-shaped cells in liquid and through low-density (0.3%) agar. On low-wetness and highdensity agar (0.75% to 2.5%), these bacteria elongate dramatically and move as a collective group on top of the surface. By comparison, the swarm motility of temperate swarmers such as Escherichia coli or Salmonella enterica is generally restricted to low-density agar (< 0.7%) or high wetness Eiken agar (reviewed in (2, 3)). For all of the aforementioned bacteria, flagella power the motility in liquid and on surfaces. Furthermore, a transition from swimming to swarming coincides with a series of large-scale transcriptional changes triggered by contact between flagella and a surface (Figure 1) (4-12).Here we utilize P. mirabilis as a tractable model for exploring how morphology and cell-cell interactions respond to the surface. P. mirabilis cells are approximately 2-µm long, rigid, and rod-shaped in liquid. Such cells swim independently, resulting in a visible uniform haze to the structure of the swim colony. Upon contact with a hard surface (Figure 1), these rigid, rod-shaped cells can elongate up to 40-fold into a flexible, snake-like, hyper-flagellated swarmer cell (13,14) that has a distinctive gene expression profile (15). P. mirabilis swarmer cells are thought to bundle their flagella to facilitate cooperative swarm motil...

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Stigmergy co-ordinates multicellular collective behaviours during Myxococcus xanthus surface migration

Cited by 31 publications

References 49 publications

Identification of the lipopolysaccharide O‐antigen biosynthesis priming enzyme and the O‐antigen ligase in Myxococcus xanthus: critical role of LPS O‐antigen in motility and development

Identification of the lipopolysaccharide O‐antigen biosynthesis priming enzyme and the O‐antigen ligase in Myxococcus xanthus: critical role of LPS O‐antigen in motility and development

Exopolysaccharides promote Myxococcus xanthus social motility by inhibiting cellular reversals

Swarming bacteria respond to increasing barriers to motility by increasing cell length and modifying colony structure

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