Bacterial Stigmergy: An Organising Principle of Multicellular Collective Behaviours of Bacteria

The self-organisation of collective behaviours often manifests as dramatic patterns of emergent large-scale order. This is true for relatively "simple" entities such as microbial communities and robot "swarms, " through to more complex self-organised systems such as those displayed by social insects, migrating herds, and many human activities. The principle of stigmergy describes those self-organised phenomena that emerge as a consequence of indirect communication between individuals of the group through the generation of persistent cues in the environment. Interestingly, despite numerous examples of multicellular behaviours of bacteria, the principle of stigmergy has yet to become an accepted theoretical framework that describes how bacterial collectives self-organise. Here we review some examples of multicellular bacterial behaviours in the context of stigmergy with the aim of bringing this powerful and elegant self-organisation principle to the attention of the microbial research community

Economic imaginaries of the Anti-biosis : between ‘economies of resistance’ and the ‘resistance of economies’

This paper seeks reports on the way economic principles, formulae and discourse inform biological research on antimicrobial resistance (AMR) in the life sciences. AMR, it can be argued, has become the basis for performing certain forms of ‘economic imaginary’. Economic imaginaries are ways of projecting and materially restructuring economic and political orders through motifs, metaphors, images and practices. The paper contributes to critical social science and humanities research on the socio-economic underpinning of biological discourse. The performance of economy in this context can be seen to follow two key trajectories. The first trajectory, discussed at length in this paper, might be described as ‘economies of resistance’. Here the language of market economics structures and frames microbiological explanations of bacterial resistance. This can be illustrated through, for example, biological theories of ‘genetic capitalism’ where capitalism itself is seen to furnish microbial life with modes of economic behaviour and conduct. ‘Economies of resistance’ are evidence of the naturalisation of socio-economic structures in expert understandings of AMR. The methodological basis of this paper lies in a historical genealogical investigation into the use of economic and market principles in contemporary microbiology. The paper reports on a corpus of published academic sources identified through the use of keywords, terms, expressions and metaphors linked to market economics. Search terms included, but were not limited to: ‘trade-off’, ‘investment’, ‘market/s’, ‘investment’, ‘competition’, ‘cooperation’, ‘economy’, ‘capital/ism’, ‘socialist/ism’, etc. ‘Economies of resistance’ complements a second distinct trajectory that can be seen to flow in the opposite direction from biology to economic politics (the ‘resistance of economies’). Here, economic imaginaries of microbial life are redeployed in large-scale debates about the nature of economic life, about the future of the welfare state, industrial strategy, and about the politics of migration and race, etc. ‘Economies of resistance’ and the ‘resistance of economies’ are not unrelated but, instead, they are mutually constituting dynamics in the co-production of AMR. In attempting to better understand this co-production, the paper draws upon literatures on the biopolitics of immunity in political philosophy and Science and Technology Studies (STS)

Biofilm mechanics: implications in infection and survival

It has long been recognized that biofilms are viscoelastic materials, however the importance of this attribute to the survival and persistence of these microbial communities is yet to be fully realized. Here we review work, which focuses on understanding biofilm mechanics and put this knowledge in the context of biofilm survival, particularly for biofilm-associated infections. We note that biofilm viscoelasticity may be an evolved property of these communities, and that the production of multiple extracellular polymeric slime components may be a way to ensure the development of biofilms with complex viscoelastic properties. We discuss viscoelasticity facilitating biofilm survival in the context of promoting the formation of larger and stronger biofilms when exposed to shear forces, promoting fluid-like behavior of the biofilm and subsequent biofilm expansion by viscous flow, and enabling resistance to both mechanical and chemical methods of clearance. We conclude that biofilm viscoelasticity contributes to the virulence of chronic biofilm infections

Mycobacterium abscessus biofilms have viscoelastic properties which may contribute to their recalcitrance in chronic pulmonary infections

Mycobacterium abscessus is emerging as a cause of recalcitrant chronic pulmonary infections, particularly in people with cystic fibrosis (CF). Biofilm formation has been implicated in the pathology of this organism, however the role of biofilm formation in infection is unclear. Two colony-variants of M. abscessus are routinely isolated from CF samples, smooth (MaSm) and rough (MaRg). These two variants display distinct colony morphologies due to the presence (MaSm) or absence (MaRg) of cell wall glycopeptidolipids (GPLs). We hypothesized that MaSm and MaRg variant biofilms might have different mechanical properties. To test this hypothesis, we performed uniaxial mechanical indentation, and shear rheometry on MaSm and MaRg colony-biofilms. We identified that MaRg biofilms were significantly stiffer than MaSm under a normal force, while MaSm biofilms were more pliant compared to MaRg, under both normal and shear forces. Furthermore, using theoretical indices of mucociliary and cough clearence, we identified that M. abscessus biofilms may be more resistant to mechanical forms of clearance from the lung, compared to other common pulmonary pathogens, such as Pseudomonas aeruginosa. Thus, the mechanical properties of M. abscessus biofilms may contribute to the persistent nature of pulmonary infections caused by this organism

Bayesian estimation of Pseudomonas aeruginosa viscoelastic properties based on creep responses of wild type, rugose, and mucoid variant biofilms

Pseudomonas aeruginosa biofilms are relevant for a variety of disease settings, including pulmonary infections in people with cystic fibrosis. Biofilms are initiated by individual bacteria that undergo a phenotypic switch and produce an extracellular polymeric slime (EPS). However, the viscoelastic characteristics of biofilms at different stages of formation and the contributions of different EPS constituents have not been fully explored. For this purpose, we develop and parameterize a mathematical model to study the rheological behavior of three biofilms — P. aeruginosa wild type PAO1, isogenic rugose small colony variant (RSCV), and mucoid variant biofilms against a range of experimental data. Using Bayesian inference to estimate these viscoelastic properties, we quantify the rheological characteristics of the biofilm EPS. We employ a Monte Carlo Markov Chain algorithm to estimate these properties of P. aeruginosa variant biofilms in comparison to those of wild type. This information helps us understand the rheological behavior of biofilms at different stages of their development. The mechanical properties of wild type biofilms change significantly over time and are more sensitive to small changes in their composition than the other two mutants

Viscoelastic properties of Pseudomonas aeruginosa variant biofilms

Pseudomonas aeruginosa evolves during chronic pulmonary infections of cystic fibrosis (CF) patients, forming pathoadapted variants that are persistent. Mucoid and rugose small-colony variants (RSCVs) are typically isolated from sputum of CF patients. These variants overproduce exopolysaccharides in the biofilm extracellular polymeric substance (EPS). Currently, changes to the biophysical properties of RSCV and mucoid biofilms due to variations in EPS are not well understood. This knowledge may reveal how lung infections resist host clearance mechanisms. Here, we used mechanical indentation and shear rheometry to analyse the viscoelasticity of RSCV and mucoid colony-biofilms compared to their isogenic parent at 2-, 4-, and 6-d. While the viscoelasticity of parental colony-biofilms underwent fluctuating temporal changes, in contrast, RSCV and mucoid colony-biofilms showed a gradual progression to more elastic-solid behaviour. Theoretical indices of mucociliary and cough clearance predict that mature 6-d parental and RSCV biofilms may show reduced cough clearance from the lung, while early mucoid biofilms may show reduced clearance by both mechanisms. We propose that viscoelasticity be considered a virulence property of biofilms

Bayesian estimation of <i>pseudomonas aeruginosa</i> viscoelastic properties based on creep of wild type, rugose, and mucoid variant biofilms

Pseudomonas aeruginosa biofilms are relevant for a variety of disease settings, including pulmonary infections in people with cystic fibrosis. Biofilms are initiated by individual bacteria that undergo a phenotypic switch and produce an extracellular polymeric slime (EPS). However, the viscoelastic characteristics of biofilms at different stages of formation and the contributions of different EPS constituents have not been fully explored. For this purpose, we develop and parameterize a mathematical model to study the rheological behavior of three biofilms — P. aeruginosa wild type PAO1, isogenic rugose small colony variant (RSCV), and mucoid variant biofilms against a range of experimental data. Using Bayesian inference to estimate these viscoelastic properties, we quantify the rheological characteristics of the biofilm EPS. We employ a Monte Carlo Markov Chain algorithm to estimate these properties of P. aeruginosa variant biofilms in comparison to those of wild type. This information helps us understand the rheological behavior of biofilms at different stages of their development. The mechanical properties of wild type biofilms change significantly over time and are more sensitive to small changes in their composition than the other two mutants

Arginine induced Streptococcus gordonii biofilm detachment using a novel 1 rotating-disc rheometry method

Oral diseases are one of the most common pathologies affecting human health. These diseases are typically associated with dental plaque-biofilms, through either build-up of the biofilm or dysbiosis of the microbial community. Arginine can disrupt dental plaque-biofilms, and maintain plaque homeostasis, making it an ideal therapeutic to combat the development of oral disease. Despite our understanding of the actions of arginine towards dental plaque-biofilms, it is still unclear how or if arginine effects the mechanical integrity of the dental plaque-biofilm. Here we adapted a rotating-disc rheometry assay, a method used to quantify marine biofilm fouling, to study how arginine treatment of Streptococcus gordonii biofilms influences biofilm detachment from surfaces. We demonstrate that the assay is highly sensitive at quantifying the presence of biofilm and the detachment or rearrangement of the biofilm structure as a function of shear stress. We demonstrate that arginine treatment leads to earlier detachment of the biofilm, indicating that arginine treatment weakens the biofilm, making it more susceptible to removal by shear stresses. Finally, we demonstrate that the biofilm disrupting affect is specific to arginine, and not a general property of amino acids, as S. gordonii biofilms treated with either glycine or lysine had mechanical properties similar to untreated biofilms. Our results add to the understanding that arginine targets biofilms by multifaceted mechanisms, both metabolic and physical, further promoting the potential of arginine as an active compound in dentifrices to maintain oral health

A combination of zinc and arginine disrupt the mechanical integrity of dental biofilms

Mechanical cleaning remains the standard of care for maintaining oral hygiene. However, mechanical cleaning is often augmented with active therapeutics that further promote oral health. A dentifrice, consisting of the “Dual Zinc plus Arginine” (DZA) technology, was found to be effective at controlling bacteria using in vitro laboratory studies, translating to clinical efficacy to deliver plaque and gingivitis reduction benefits. Here we used biophysical analyses and confocal laser scanning microscopy, to understand how DZA dentifrice impacted the mechanical properties of dental plaque biofilms, with the objective of determining if changes to biofilm rheology enhances the removal of dental plaque. Using both uniaxial mechanical indentation and an adapted rotating-disc rheometry assay, it was found that DZA treatment compromised biofilm mechanical integrity, resulting in the biofilm being more susceptible to removal by shear forces, when compared to treatment with either arginine or zinc alone. Confocal laser scanning microscopy revealed that DZA treatment reduced the amount of extracellular polymeric slime within the biofilm, likely accounting for the reduced mechanical properties. We propose a model where arginine facilitates the entry of zinc into the biofilm, resulting in additive effects of the two activities towards dental plaque biofilms. Together, our results support the use of a dentifrice containing the Dual Zinc plus Arginine as part of daily oral hygiene regimens