Metabolic basis of brain-like electrical signalling in bacterial communities

Abstract

Information processing in the mammalian brain relies on a careful regulation of the membrane potential dynamics of its constituent neurons, which propagates across the neuronal tissue via electrical signalling. We recently reported the existence of electrical signalling in a much simpler organism, the bacterium Bacillus subtilis. In dense bacterial communities known as biofilms, nutrient-deprived B. subtilis cells in the interior of the colony use electrical communication to transmit stress signals to the periphery, which interfere with the growth of peripheral cells and reduce nutrient consumption, thereby relieving stress from the interior. Here we explicitly address the interplay between metabolism and electrophysiology in bacterial biofilms, by introducing a spatially-extended mathematical model that combines the metabolic and electrical components of the phenomenon in a discretised reaction-diffusion scheme. The model is experimentally validated by environmental and genetic perturbations, and confirms that metabolic stress is transmitted through the bacterial population via a potassium wave. Interestingly, this behaviour is reminiscent of cortical spreading depression in the brain, characterised by a wave of electrical activity mediated by potassium diffusion that has been linked to various neurological disorders, calling for future studies on the evolutionary link between the two phenomena.

Reframing cognition: getting down to biological basics

“…In a study of the interplay between metabolism and electrical signalling, the group found that metabolic stress is transmitted through a biofilm via a potassium wave, which regulates the membrane potential of B. subtilis cells in ways similar to neurons in the mammalian brain. The behaviour produced in the biofilm, the team noted, ‘is reminiscent of cortical spreading depression in the brain’, which is also ‘characterized by a wave of electrical activity mediated by potassium diffusion that has been linked to various neurological disorders’ [18]. Perhaps not surprisingly, they suggested future research into ‘the evolutionary link between the two phenomena’, electrical signalling in bacterial biofilms and information-processing in mammalian brains.…”

Valuing what happens: a biogenic approach to valence and (potentially) affect

“…habituation and sensitization) and associative learning (e.g. classical conditioning), and are implemented on various time-scales and levels of biological organization, from fast responses of aneural bioelectric and metabolic levels [29] to slower responses on the level of gene regulation [109]. Learning in these contexts involves not only changes in adaptation but also prediction of environmental stimuli, which goes well beyond traditional formulations of homeostasis.…”

“…Bacterial ion channels provided insights into the operation of ion channels in neurons, and were the basis for a Nobel Prize, 2 long before their function in microbes was known. Only relatively recently a team of researchers in Gürol Süel's laboratory at the University of California (San Diego) discovered the function of ion channel-based electrical signalling in structured communities of Bacillus subtilis is similar to that in neurons: propagating information over long distances and large numbers of cells [28], in this case for the purposes of regulating metabolism between the centre and the periphery of the growing colony [29,30]. These surprising discoveries have led to more results.…”

Understanding the evolution of interspecies interactions in microbial communities

“…For example, it may not be possible to 66 predict from growing each species by itself what the joint reproductive output of a collective 67 will be, or how robust such a collective will be to external biotic and abiotic perturbations. 68Microbial communities can also perform chemical transformations that would be impossible 69 for one individual species to achieve[16], and some communities even display complex 70 behaviours such as collective motion and electrochemical signalling, which have traditionally 71 been associated with higher organisms [17,18]. 72…”

“…Microbial communities can also perform chemical transformations that would be impossible 69 for one individual species to achieve[16], and some communities even display complex 70 behaviours such as collective motion and electrochemical signalling, which have traditionally 71 been associated with higher organisms [17,18]. 72…”