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...sed systems that arise through an individual of the collective influencing the movement or behaviour of other individuals at a later point in time through the generation of persistent cues within the environment [5, 6]. The concept of stigmergy was first introduced by the entomologist Grasse in 1959 to explain the construction of termite colonies [5]. This powerful concept, for the first time, explained how apparently random and independent movements of an individual could result in the transfer of persistent information locally, thereby manifesting as coordinated behaviour at a global level [2, 6]. The principle of stigmergy has since been employed to describe a vast array of group activities such as the laying-down of pheromone trails by foraging ants, herd migration in animals, and various aspects of human activities including the following of hiking trails and pedestrian footpaths [7–11] as well as artificial systems such as “swarm intelligence” within robotics and computing [12–17]. Interestingly, even the development of multicellular tissues has been described as a stigmergic phenomenon in which chemical cues are embedded in extracellular matrix material [18]. As other scientific ...

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...g motility and the slime encasement facilitates the maintenance of a cohesive organisation of cells [42, 44]. Therefore slime production and slime trail following promote the self-organisation of collective behaviours necessary for the expansion of the swarming colony. Gliding motility of Myxococcus xanthus is mediated by the combined efforts of two motility modes; social (S) motility and adventurous (A) motility. Similar to twitching motility, S-motility is driven by the extension, binding, and retraction of tfp with this motility mode being typically displayed by groups or clusters of cells [45, 46]. A-motility mediates single cell migration and in contrast to that of S-motility, the machinery driving A-motility is yet to be confirmed and is an area of controversy [47, 48]. However all current schools of thought predict the role of a secreted slime in facilitating the A-motility of this organism [49– 51], where phase bright trails are observed at the leading edge of the M. xanthus swarms when grown on semisolid media (Figure 1(e); [52]), similar to that of Pr. mirabilis. M. xanthus cells preferentially migrate along these slime trails, with cells frequently observed to turn onto the trai...

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...la-mediated swarmingmotility of Proteus spp. leads to the formation of rapidly expanding colonies grown on agar that are characterised by a repeated concentric circle pattern that extends across the swarm.This patterning is attributed to continuous rounds of cell differentiation, where the normal rod cells, which are largely nonmotile, differentiate into long, hyperflagellated swarmer cells. As a collective these swarmer cells rapidly migrate across the surface until they differentiate back to the nonmotile normal cells resulting in consolidation and the formation of the observed ring pattern [41, 42]. The flagella of Proteus swarmer cells interweave with flagella from the same cell and with those of neighbouring cells, forming a connected and highly synchronised swarming front that aids in the rapid expansion by these colonies [43]. The secretion of an extracellular slime has been found to facilitate the collective swarming behaviour of Pr. mirabilis. At the leading edge of Pr. mirabilis swarms, swarmer cells are encased in a slime layer and appear to preferentially move along an interconnected network of phase bright slime trails (Figure 1(d); [44]). It has been hypothesised that the sli...

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...ver all current schools of thought predict the role of a secreted slime in facilitating the A-motility of this organism [49– 51], where phase bright trails are observed at the leading edge of the M. xanthus swarms when grown on semisolid media (Figure 1(e); [52]), similar to that of Pr. mirabilis. M. xanthus cells preferentially migrate along these slime trails, with cells frequently observed to turn onto the trails rather than migrating across virgin territory. Continued cellular traffic along the trails results in their thickening and extension as a consequence of continued slime deposition [51, 53]. It is recognised that this trail following behaviour coordinates the collective behaviour of M. xanthus cells, specifically those displaying A-motility, at the leading edge of the surface swarms, and contributes to the emergence of the interconnected pattern networks at these areas [51–53]. The following of slime trails duringPr.mirabilis swarming and M. xanthus gliding motilities are both sematectonic and quantitative stigmergic systems, where the stimulus (slime) is a physical manifestation within the environment that directly contributes to the expansion of the community as it is required...

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...la-mediated swarmingmotility of Proteus spp. leads to the formation of rapidly expanding colonies grown on agar that are characterised by a repeated concentric circle pattern that extends across the swarm.This patterning is attributed to continuous rounds of cell differentiation, where the normal rod cells, which are largely nonmotile, differentiate into long, hyperflagellated swarmer cells. As a collective these swarmer cells rapidly migrate across the surface until they differentiate back to the nonmotile normal cells resulting in consolidation and the formation of the observed ring pattern [41, 42]. The flagella of Proteus swarmer cells interweave with flagella from the same cell and with those of neighbouring cells, forming a connected and highly synchronised swarming front that aids in the rapid expansion by these colonies [43]. The secretion of an extracellular slime has been found to facilitate the collective swarming behaviour of Pr. mirabilis. At the leading edge of Pr. mirabilis swarms, swarmer cells are encased in a slime layer and appear to preferentially move along an interconnected network of phase bright slime trails (Figure 1(d); [44]). It has been hypothesised that the sli...

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... particularly the case for the slime mediating the A-motility of M. xanthus (sematectonic stigmergy). Continued traffic along the slime trails amplifies the slime deposited resulting in further recruitment of cells migrating along these regions (quantitative stigmergy). It has been shown recently that the formation of vortexes comprised of thousands of bacteria rotating in unison that occur during active surface migration by Paenibacillus vortex biofilms occurs as a consequence of the actions of a subpopulation of filamentous cells that direct the motion of the other members of the collective [54, 55]. This appears to be another example of bacterial stigmergy, though it remains to be determined if this collective behaviour occurs as a consequence of physical alteration of the environment, slime, or chemical cues. Scientifica 5 A number of computational models have been developed to describe collective behaviours displayed during swarm activities, particularly for M. xanthus [56–58]. Due to the inherent difficulties in modelling biological systems, a number of these models do not truly reflect experimental observations or contain artefacts as a consequence of the rule parameters incorporate...

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...ver all current schools of thought predict the role of a secreted slime in facilitating the A-motility of this organism [49– 51], where phase bright trails are observed at the leading edge of the M. xanthus swarms when grown on semisolid media (Figure 1(e); [52]), similar to that of Pr. mirabilis. M. xanthus cells preferentially migrate along these slime trails, with cells frequently observed to turn onto the trails rather than migrating across virgin territory. Continued cellular traffic along the trails results in their thickening and extension as a consequence of continued slime deposition [51, 53]. It is recognised that this trail following behaviour coordinates the collective behaviour of M. xanthus cells, specifically those displaying A-motility, at the leading edge of the surface swarms, and contributes to the emergence of the interconnected pattern networks at these areas [51–53]. The following of slime trails duringPr.mirabilis swarming and M. xanthus gliding motilities are both sematectonic and quantitative stigmergic systems, where the stimulus (slime) is a physical manifestation within the environment that directly contributes to the expansion of the community as it is required...

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...] to quantitate the behaviour of the individual cells in the absence and presence of DNaseI. Interrogation of the resulting image informatics database revealed that eDNA facilitates twitching motility-mediated biofilm expansion by enabling more frequent movements of individual cells, thereby resulting in more sustained motion and greater distances traversed by individual cells over longer time periods. These analyses also revealed that eDNA is required for maintaining coherent cell behaviour and cell alignment over time [28]. Previous reports have identified that P. aeruginosa tfp bind to DNA [39] and that P. aeruginosa cells spontaneously pneumatically orient with the direction of extended DNA chains in a matrix of aligned, concentrated DNA [40]. We proposed that the bed of aligned eDNA molecules within P. aeruginosa interstitial biofilms maintains cell orientations by aligning cells to the thin strands of eDNA and that eDNA provides a substrate for optimal tfp binding, consequently enabling more frequent tfp-powered translocations, ensuring smooth traffic flow within the trail network and a consistent supply of cells to the leading edge of the expanding biofilm [28]. We also propose ...

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...ntinuous rounds of cell differentiation, where the normal rod cells, which are largely nonmotile, differentiate into long, hyperflagellated swarmer cells. As a collective these swarmer cells rapidly migrate across the surface until they differentiate back to the nonmotile normal cells resulting in consolidation and the formation of the observed ring pattern [41, 42]. The flagella of Proteus swarmer cells interweave with flagella from the same cell and with those of neighbouring cells, forming a connected and highly synchronised swarming front that aids in the rapid expansion by these colonies [43]. The secretion of an extracellular slime has been found to facilitate the collective swarming behaviour of Pr. mirabilis. At the leading edge of Pr. mirabilis swarms, swarmer cells are encased in a slime layer and appear to preferentially move along an interconnected network of phase bright slime trails (Figure 1(d); [44]). It has been hypothesised that the slime trails aid in directing swarming motility and the slime encasement facilitates the maintenance of a cohesive organisation of cells [42, 44]. Therefore slime production and slime trail following promote the self-organisation of collec...

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...self-organisation and emergent pattern networks of bacterial swarms. 3. Bacterial Biofilms Bacterial biofilms are multicellular communities of bacteria that are attached to each other and often a biotic or abiotic surface via a self-produced extracellular matrix comprised of extracellular polymeric substances (EPS) including exopolysaccharides, eDNA, proteins, and lipids [60–62]. The production of this EPSmatrix is essential for biofilm development as it provides intercellular connectivity that binds cells to each other and, in the case of surface-attached biofilms, provides surface adherence [60, 61]. The ability of the EPS matrix produced by biofilm cells to promote cohesion and surface attachment of the biofilm community is an example of sematectonic stigmergy. It has been observed that individual P. aeruginosa cells undergo extensive twitching motility-mediated surface exploration prior to subsequent microcolony formation during the early stages of biofilm formation on glass submerged in liquid nutrient media [63–66]. Zhao and colleagues showed recently that, during surface exploration, P. aeruginosa cells deposited trails of the exopolysaccharide Psl, which appeared to recruit additio...

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...mation of the observed ring pattern [41, 42]. The flagella of Proteus swarmer cells interweave with flagella from the same cell and with those of neighbouring cells, forming a connected and highly synchronised swarming front that aids in the rapid expansion by these colonies [43]. The secretion of an extracellular slime has been found to facilitate the collective swarming behaviour of Pr. mirabilis. At the leading edge of Pr. mirabilis swarms, swarmer cells are encased in a slime layer and appear to preferentially move along an interconnected network of phase bright slime trails (Figure 1(d); [44]). It has been hypothesised that the slime trails aid in directing swarming motility and the slime encasement facilitates the maintenance of a cohesive organisation of cells [42, 44]. Therefore slime production and slime trail following promote the self-organisation of collective behaviours necessary for the expansion of the swarming colony. Gliding motility of Myxococcus xanthus is mediated by the combined efforts of two motility modes; social (S) motility and adventurous (A) motility. Similar to twitching motility, S-motility is driven by the extension, binding, and retraction of tfp with th...

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...lf-organisation of collective behaviours necessary for the expansion of the swarming colony. Gliding motility of Myxococcus xanthus is mediated by the combined efforts of two motility modes; social (S) motility and adventurous (A) motility. Similar to twitching motility, S-motility is driven by the extension, binding, and retraction of tfp with this motility mode being typically displayed by groups or clusters of cells [45, 46]. A-motility mediates single cell migration and in contrast to that of S-motility, the machinery driving A-motility is yet to be confirmed and is an area of controversy [47, 48]. However all current schools of thought predict the role of a secreted slime in facilitating the A-motility of this organism [49– 51], where phase bright trails are observed at the leading edge of the M. xanthus swarms when grown on semisolid media (Figure 1(e); [52]), similar to that of Pr. mirabilis. M. xanthus cells preferentially migrate along these slime trails, with cells frequently observed to turn onto the trails rather than migrating across virgin territory. Continued cellular traffic along the trails results in their thickening and extension as a consequence of continued slime depos...

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...lf-organisation of collective behaviours necessary for the expansion of the swarming colony. Gliding motility of Myxococcus xanthus is mediated by the combined efforts of two motility modes; social (S) motility and adventurous (A) motility. Similar to twitching motility, S-motility is driven by the extension, binding, and retraction of tfp with this motility mode being typically displayed by groups or clusters of cells [45, 46]. A-motility mediates single cell migration and in contrast to that of S-motility, the machinery driving A-motility is yet to be confirmed and is an area of controversy [47, 48]. However all current schools of thought predict the role of a secreted slime in facilitating the A-motility of this organism [49– 51], where phase bright trails are observed at the leading edge of the M. xanthus swarms when grown on semisolid media (Figure 1(e); [52]), similar to that of Pr. mirabilis. M. xanthus cells preferentially migrate along these slime trails, with cells frequently observed to turn onto the trails rather than migrating across virgin territory. Continued cellular traffic along the trails results in their thickening and extension as a consequence of continued slime depos...

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...ity. A recent review has called for the employment of a more integrative approach across scientific fields in the study of self-organising systems [71]. Stigmergy provides an excellent example of this approach where, since its first introduction within the field of entomology [5], the importance of this concept has been recognised across diverse areas ranging from biology to social sciences, technology, and computer sciences [15, 16, 72]. The wide acceptance of stigmergy can, for the most 6 Scientifica part, be attributed to a special edition of Artificial Life dedicated to stigmergic systems [6, 73], with the hopes of bringing this concept to the forefront within the scientific community. This concept, despite its obvious application to the understanding of multicellular bacterial behaviours, has been largely overlooked within the field of microbiology. Here we recognise the importance of the concept of stigmergic self-organisation and the implications it has on understanding the collective behaviours of complex multicellular bacterial communities. We propose that bacterial stigmergy should be included in the repertoire of systems that bacteria employ to control multicellular activities....

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...ng exopolysaccharide trails to coordinate the single cellular motilities of P. aeruginosa during early biofilm development is an example of sematectonic and quantitative stigmergy. Zhao et al. used a “rich-gettingricher” analogy comparable to that of capitalist economies to describe this emergent behaviour [67], which has itself been described as a stigmergic system [15, 16]. 4. Quorum Sensing In many bacterial communities quorum sensing regulates and coordinates social behaviours, such as bioluminescence, secretion of public goods, and the switch from planktonic to the biofilm mode of growth [69]. Quorum sensing occurs through the release of small molecules by individual bacteria into the environment by passive diffusion. The concentration of these small molecules increases within the environment with increasing cell density, permitting cells to gather information about their surrounding neighbours. Once a sufficient quantity of signal is present within the environment, reflecting a critical population density, a gene regulation cascade is initiated culminating in the up- or downregulation of the expression of various genes required for social behaviours, virulence factor production, ...

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...ing occurs through the release of small molecules by individual bacteria into the environment by passive diffusion. The concentration of these small molecules increases within the environment with increasing cell density, permitting cells to gather information about their surrounding neighbours. Once a sufficient quantity of signal is present within the environment, reflecting a critical population density, a gene regulation cascade is initiated culminating in the up- or downregulation of the expression of various genes required for social behaviours, virulence factor production, and so forth [69, 70]. In this manner it has been identified that quorum sensing can regulate the expression of over 300 genes within P. aeruginosa [69]. Quorum sensing within bacterial communities bares a striking resemblance to pheromone signalling that coordinates the collective behaviours of social insects. It is therefore interesting to speculate whether quorum sensing offers another example of stigmergic self-organisationwithin bacterial communities. Under circumstances where quorum sensing signalling molecules are able to persist and accumulate within the environment, then quorum sensing could be considered...

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...ity is an example of sematectonic stigmergy. It has been observed that individual P. aeruginosa cells undergo extensive twitching motility-mediated surface exploration prior to subsequent microcolony formation during the early stages of biofilm formation on glass submerged in liquid nutrient media [63–66]. Zhao and colleagues showed recently that, during surface exploration, P. aeruginosa cells deposited trails of the exopolysaccharide Psl, which appeared to recruit additional cells along these trails leading to a positive feedback loop of further Psl deposition and subsequent cell attraction [67]. It was hypothesised that this trail following behaviour was facilitated by twitchingmotility-mediated surface exploration, where the tfp were thought to probe the surrounding areas for Psl networks, promoting binding of the tfp and directing cellular migration to these areas [67]. In areas of high Psl concentration, cells were observed to adhere to the substratum and correlated to the subsequent sites of microcolony formation [67, 68]. This mechanism of following exopolysaccharide trails to coordinate the single cellular motilities of P. aeruginosa during early biofilm development is an exam...

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...ide Psl, which appeared to recruit additional cells along these trails leading to a positive feedback loop of further Psl deposition and subsequent cell attraction [67]. It was hypothesised that this trail following behaviour was facilitated by twitchingmotility-mediated surface exploration, where the tfp were thought to probe the surrounding areas for Psl networks, promoting binding of the tfp and directing cellular migration to these areas [67]. In areas of high Psl concentration, cells were observed to adhere to the substratum and correlated to the subsequent sites of microcolony formation [67, 68]. This mechanism of following exopolysaccharide trails to coordinate the single cellular motilities of P. aeruginosa during early biofilm development is an example of sematectonic and quantitative stigmergy. Zhao et al. used a “rich-gettingricher” analogy comparable to that of capitalist economies to describe this emergent behaviour [67], which has itself been described as a stigmergic system [15, 16]. 4. Quorum Sensing In many bacterial communities quorum sensing regulates and coordinates social behaviours, such as bioluminescence, secretion of public goods, and the switch from planktonic to ...

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...g motility and the slime encasement facilitates the maintenance of a cohesive organisation of cells [42, 44]. Therefore slime production and slime trail following promote the self-organisation of collective behaviours necessary for the expansion of the swarming colony. Gliding motility of Myxococcus xanthus is mediated by the combined efforts of two motility modes; social (S) motility and adventurous (A) motility. Similar to twitching motility, S-motility is driven by the extension, binding, and retraction of tfp with this motility mode being typically displayed by groups or clusters of cells [45, 46]. A-motility mediates single cell migration and in contrast to that of S-motility, the machinery driving A-motility is yet to be confirmed and is an area of controversy [47, 48]. However all current schools of thought predict the role of a secreted slime in facilitating the A-motility of this organism [49– 51], where phase bright trails are observed at the leading edge of the M. xanthus swarms when grown on semisolid media (Figure 1(e); [52]), similar to that of Pr. mirabilis. M. xanthus cells preferentially migrate along these slime trails, with cells frequently observed to turn onto the trai...

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...o be another example of bacterial stigmergy, though it remains to be determined if this collective behaviour occurs as a consequence of physical alteration of the environment, slime, or chemical cues. Scientifica 5 A number of computational models have been developed to describe collective behaviours displayed during swarm activities, particularly for M. xanthus [56–58]. Due to the inherent difficulties in modelling biological systems, a number of these models do not truly reflect experimental observations or contain artefacts as a consequence of the rule parameters incorporated into themodel [59]. Stigmergic systems have long been the focus of extensive computational modelling to understand the emergent properties within these systems [7–10] and to relate stigmergic principles from one system to another in an attempt to draw comparisons from well-studied and established systems [17]. It is our contention that a similar approach could be taken for modelling bacterial swarming communities through the incorporation of key ideas from other stigmergic models, such as those of Helbing et al. and Goldstone et al., who modelled sematectonic and quantitative stigmergic systems such as trail fo...

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...bove examples. This highlights the conserved nature of self-organising mechanisms within nature regardless of the cognitive abilities of the individual entities and suggests a common evolution of trail following as a simple yet effective means of coordinating collective behaviours. The idea that self-organising systems utilised by bacterial communities are similar to those utilised by higher organisms is gaining interest within the scientific community. A recent review has called for the employment of a more integrative approach across scientific fields in the study of self-organising systems [71]. Stigmergy provides an excellent example of this approach where, since its first introduction within the field of entomology [5], the importance of this concept has been recognised across diverse areas ranging from biology to social sciences, technology, and computer sciences [15, 16, 72]. The wide acceptance of stigmergy can, for the most 6 Scientifica part, be attributed to a special edition of Artificial Life dedicated to stigmergic systems [6, 73], with the hopes of bringing this concept to the forefront within the scientific community. This concept, despite its obvious application to the...

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... The idea that self-organising systems utilised by bacterial communities are similar to those utilised by higher organisms is gaining interest within the scientific community. A recent review has called for the employment of a more integrative approach across scientific fields in the study of self-organising systems [71]. Stigmergy provides an excellent example of this approach where, since its first introduction within the field of entomology [5], the importance of this concept has been recognised across diverse areas ranging from biology to social sciences, technology, and computer sciences [15, 16, 72]. The wide acceptance of stigmergy can, for the most 6 Scientifica part, be attributed to a special edition of Artificial Life dedicated to stigmergic systems [6, 73], with the hopes of bringing this concept to the forefront within the scientific community. This concept, despite its obvious application to the understanding of multicellular bacterial behaviours, has been largely overlooked within the field of microbiology. Here we recognise the importance of the concept of stigmergic self-organisation and the implications it has on understanding the collective behaviours of complex multicellula...

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...8]. We observed that P. aeruginosa interstitial biofilms contain eDNA distributed either as a fine coating of the cells or as concentrated, punctate foci from which thin tendrils radiated in the overall direction of the motion of cells (Figure 1(c); [28]). Removal of this eDNA, through the incorporation of the eDNA-degrading enzyme DNaseI into the solidified nutrient media, resulted in the abrogation of the characteristic interconnected pattern network of these biofilms [28]. To understand the role of eDNA within these biofilms we employed a computer vision and cell tracking analysis pipeline [28, 37, 38] to quantitate the behaviour of the individual cells in the absence and presence of DNaseI. Interrogation of the resulting image informatics database revealed that eDNA facilitates twitching motility-mediated biofilm expansion by enabling more frequent movements of individual cells, thereby resulting in more sustained motion and greater distances traversed by individual cells over longer time periods. These analyses also revealed that eDNA is required for maintaining coherent cell behaviour and cell alignment over time [28]. Previous reports have identified that P. aeruginosa tfp bind to DNA [...

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...evealed that eDNA facilitates twitching motility-mediated biofilm expansion by enabling more frequent movements of individual cells, thereby resulting in more sustained motion and greater distances traversed by individual cells over longer time periods. These analyses also revealed that eDNA is required for maintaining coherent cell behaviour and cell alignment over time [28]. Previous reports have identified that P. aeruginosa tfp bind to DNA [39] and that P. aeruginosa cells spontaneously pneumatically orient with the direction of extended DNA chains in a matrix of aligned, concentrated DNA [40]. We proposed that the bed of aligned eDNA molecules within P. aeruginosa interstitial biofilms maintains cell orientations by aligning cells to the thin strands of eDNA and that eDNA provides a substrate for optimal tfp binding, consequently enabling more frequent tfp-powered translocations, ensuring smooth traffic flow within the trail network and a consistent supply of cells to the leading edge of the expanding biofilm [28]. We also propose that eDNA serves as an intercellular “glue” that binds the cells togetherwithin vanguard raft assemblages thereby facilitating coherent cell movements t...

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... particularly the case for the slime mediating the A-motility of M. xanthus (sematectonic stigmergy). Continued traffic along the slime trails amplifies the slime deposited resulting in further recruitment of cells migrating along these regions (quantitative stigmergy). It has been shown recently that the formation of vortexes comprised of thousands of bacteria rotating in unison that occur during active surface migration by Paenibacillus vortex biofilms occurs as a consequence of the actions of a subpopulation of filamentous cells that direct the motion of the other members of the collective [54, 55]. This appears to be another example of bacterial stigmergy, though it remains to be determined if this collective behaviour occurs as a consequence of physical alteration of the environment, slime, or chemical cues. Scientifica 5 A number of computational models have been developed to describe collective behaviours displayed during swarm activities, particularly for M. xanthus [56–58]. Due to the inherent difficulties in modelling biological systems, a number of these models do not truly reflect experimental observations or contain artefacts as a consequence of the rule parameters incorporate...

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... aeruginosa when they are grown at the interstitial space between the petri dish andmedia [36]. However, whether this emergent pattern arises due to the corrosion of the agar during biofilm expansion, creating furrows that guide the movements of the bacteria remains to be determined. The agar pitting phenotypes of bothD. nodosus andMoraxella bovis have been correlated with the presence of tfp. It has been speculated that the agar polysaccharides may act as ligands to which the tfp bind and that the physical interaction of the tfp with the agar may be responsible for the agar pitting phenotype [32]. It is interesting to speculate that the formation of furrownetworks may constitute a more global mechanism for the stigmergic organisation of bacterial communities. We have recently also identified a role for extracellular DNA (eDNA) in coordinating the collective behaviour of Scientifica 3 (a) 0 100 200 (nm) 200.0 100.0 0.0 (nm ) 60.0 45.0 30.0 15.0 0.0 0.0 0.0 15.0 30.0 45.0 60.0 (...