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Stigmergy a Key Driver of Self-Organization in Bacterial Biofilms

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Stigmergy a Key Driver of Self-Organization in Bacterial Biofilms ARTICLE ADDENDUM ARTICLEARTICLE ADDENDUMADDENDUM Communicative & Integrative Biology 6:6, e27557; November/December; © 2013 Landes Bioscience Stigmergy A key driver of self-organization in bacterial biofilms Erin S Gloag1, Muhammad A Javed2, Huabin Wang3, Michelle L Gee3, Scott A Wade2, Lynne Turnbull1, and Cynthia B Whitchurch1* 1The ithree institute; University of Technology Sydney; Ultimo, NSW Australia; 2Faculty of Engineering and Industrial Sciences; Biotactical Engineering; IRIS; Swinburne University of Technology; Hawthorn, VIC Australia; 3School of Chemistry; University of Melbourne; Parkville, VIC Australia acterial biofilms are complex multi- can be included in the repertoire of sys- Bcellular communities that are often tems used by bacteria to coordinate com- associated with the emergence of large- plex multicellular behaviors. scale patterns across the biofilm. How The study of the emergence of large- bacteria self-organize to form these struc- scale pattern formation in biotic and abi- tured communities is an area of active otic systems is of broad scientific interest. research. We have recently determined Within biological systems pattern forma- that the emergence of an intricate network tion is a consequence of self-organization of trails that forms during the twitching and collective motion displayed by the indi- motility mediated expansion of Pseudo- vidual organisms belonging to a system or monas aeruginosa biofilms is attributed group.1,2 Collective behaviors are observed to an interconnected furrow system that ubiquitously in nature from higher ani- is forged in the solidified nutrient media mals such as flocks of birds, schools of fish, by aggregates of cells as they migrate social behaviors of ants and termites and across the media surface. This network herd migrations through to group behav- acts as a means for self-organization of iors observed in communities of microor- collective behavior during biofilm expan- ganisms such as the active expansion of sion as the cells following these vanguard bacterial biofilms. It has been speculated aggregates were preferentially confined that the emergence of self-organized pat- Keywords: Self-organisation, twitching within the furrow network resulting in tern formation offers adaptive advantages motility, biofilms, collective behaviour, the formation of an intricate network of for the system to respond to the surround- Pseudomonas aeruginosa trails of cells. Here we further explore the ing environment.1,3 *Correspondence to: Cynthia Whitchurch; process by which the intricate network of A common feature often displayed by Email: [email protected] trails emerges. We have determined that these collective phenomena is the forma- Submitted: 11/09/2013 the formation of the intricate network tion of trails that lead to the emergence Accepted: 11/25/2013 of furrows is associated with significant of dramatic patterns of large-scale order.4 Citation: Gloag ES, Javed MA, Wang H, Gee ML, remodeling of the sub-stratum underly- This is true for the development of bacte- Wade SA, Turnbull L, Whitchurch CB. Stigmergy: ing the biofilm. The concept of stigmergy rial communities, which are often char- A key driver of self-organization in bacterial has been used to describe a variety of self- acterized by extensive spatiotemporal biofilms. Communicative & Integrative Biology organization processes observed in higher patterns and multicellular structures.1,2,5-8 2013; 6:e27331; http://dx.doi.org/10.4161/cib.27331 organisms and abiotic systems that involve Understanding the mechanisms that gov- indirect communication via persistent ern the self-organized behaviors that lead to Addendum to: Gloag ES, Turnbull L, Huang A, Vallotton P, Wang H, Nolan LM, Mililli L, Hunt cues in the environment left by individu- the emergence of these patterns is an area of 2,3,8,9 C, Lu J, Osvath SR, et al. Self-organization of als that influence the behavior of other active research. bacterial biofilms is facilitated by extracellular individuals of the group at a later point An example of the self-organized emer- DNA. Proc Natl Acad Sci U S A 2013; 110:11541- in time. We propose that the concept of gence of striking patterns in bacterial 6; http://dx.doi.org/10.1073/pnas.1218898110; stigmergy can also be applied to describe communities is observed at the edges of PMID:23798445 self-organization of bacterial biofilms and actively expanding biofilms of Pseudomonas www.landesbioscience.com Communicative & Integrative Biology e27557-1 aeruginosa when cultured at the interface of optical profilometry to visualize the topog- furrows in the older lattice network located solidified nutrient media and a coverslip. raphy of the substrate beneath the biofilm. further back in the biofilm (Fig. 1A and Under these conditions, the biofilms rap- This technique confirmed our previous E). In contrast, the lattice furrows have idly expand via type IV pili (tfp)-mediated observations that the substrate underlying low walls and bases that are situated higher twitching motility producing an extensive the interstitial biofilm contains an intricate than that of the leading edge furrows and intricate interconnected network of network of furrows (Fig. 1A). However, (Fig. 1A and E). These observations sug- cells.10,11 We recently set out to investigate in this study we were able to correlate the gest that the formation of the intricate fur- how these actively expanding P. aeruginosa field of view obtained with phase contrast row network is associated with significant biofilm communities self-organize to pro- microscopy with the 3D optical profilom- remodeling of the semi-solid media that duce such dramatic large-scale patterns.11 eter image of the same region. As shown occurs when new intersections are forged, We found that during active biofilm expan- in Figure 1A-C, the network of trails of resulting in the formation of an intricate sion, cells self-organize into highly aligned cells of the interstitial biofilm correlates interconnected network of narrow furrows aggregates (rafts) that plough a network of extremely well with the underlying furrow with shallow walls. Interestingly, both our interconnected furrows which physically system such that the phase contrast image AFM and 3D optical profilometry data confine the following cells, resulting in the of the cellular trail network fits easily were obtained several days after removal emergence of the lattice-like network of within the 3D optical profilometer image of the cells from the media. This indicates trails that is a characteristic feature of these of the underlying furrow network (Fig. 1B that the furrow network is a consequence biofilms.11 Here we have further explored and C). of physical changes in the media such that the process by which the intricate network We have also performed a detailed anal- in the absence of cells the media does not of trails is formed in actively expanding ysis of furrow widths using data obtained return to its original state. interstitial biofilms of P. aeruginosa. with both 3D optical profilometry and P. aeruginosa interstitial biofilm Refinement of the trail network AFM. Both techniques yielded equiva- expansion is mediated by stigmergic remodels the semi-solid substratum lent values and indicate that the widths self-organization In our previous study, we utilized tap- are narrower in the furrows of the lattice Stigmergy is a mechanism of self- ping mode atomic force microscopy (AFM) network compared with the furrows at the organization that was first introduced by to image and analyze the furrows within outermost regions of the biofilm (Fig. 1D). the French entomologist Grassé in 1959 the semi-solid media once the cells had We found that the widths of the furrows to describe the social behaviors of insects been removed via washing.11 However, our beneath the raft head and raft trails were such as ants and termites.12 It is a con- AFM imaging system was limited to a rela- equivalent (mean widths of 18.79 ± 6.52 cept used to describe self-organization tively small scan size and we were unable to μm and 18.50 ± 6.33 μm, respectively) of group activities via mechanisms that accurately correlate AFM scan regions with whereas the widths of the furrows in the involve indirect communication medi- specific regions of the biofilm visualized by network behind the rafts and in the older, ated by alteration of the environment. phase-contrast microscopy. To overcome more intricate lattice network became pro- The underlying principle of stigmergy is these limitations, in this study we have uti- gressively narrower (furrow mean width that by modifying the local environment, lized correlative phase-contrast microscopy of 12.07 ± 4.37 μm and 8.20 ± 2.40 μm, an individual can indirectly influence the and 3D optical profilometry. The latter is respectively; Figure 1D). These observa- actions of another individual at a later a non-contact mode of imaging that per- tions suggest that sustained cellular traf- time thereby leading to the emergence of mits visualization of a large area and thus fic through the network refines the wider apparently coordinated collective behav- enables acquisition of a “birds-eye” over- channels forged by the advancing rafts. ior, accounting for the formation of com- view of the furrow network beneath the We expected that the impact of sus- plex structures, even by relatively simple expanding biofilm. tained cellular traffic throughout the net- “agents” that lack self-awareness or plan- In this study we employed
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