Engineering microbial communities using thermodynamic principles and electrical interfaces

Abstract

Microbial communities present the next research frontier. We argue here that understanding and engineering microbial communities requires a holistic view that considers not only species-species, but also species-environment interactions, and feedbacks between ecological and evolutionary dynamics (eco-evo feedbacks). Due this multi-level nature of interactions, we predict that approaches aimed soley at altering specific species populations in a community (through strain enrichment or inhibition), would only have a transient impact, and species-environment and eco-evo feedbacks would eventually drive the microbial community to its original state. We propose a higher-level engineering approach that is based on thermodynamics of microbial growth, and that considers specifically microbial redox biochemistry. Within this approach, the emphasis is on enforcing specific environmental conditions onto the community. These are expected to generate higher-level thermodynamic bounds onto the system, which the community structure and function can then adapt to. We believe that the resulting end-state can be ecologically and evolutionarily stable, mimicking the natural states of complex communities. Toward designing the exact nature of the environmental enforcement, thermodynamics and redox biochemistry can act as coarse-grained principles, while the use of electrodes-as electron providing or accepting redox agents-can provide implementation with spatiotemporal control.

Soluble electron acceptors affect bioluminescence from Shewanella woodyi

“…These electron acceptors were chosen because of their overlapping electrochemical potential window in saltwater medium. This electrochemical window is also consistent with common redox pairs involved in intracellular metabolism . In addition, bidirectional bacterial electron transfer can be influenced by the concentration of nitrate, while Co(II) ions are a low‐redox potential heavy metal suitable for affecting the electrochemical processes in the cell.…”

“…In general, there was a nonlinear decrease in the luminescence generated from the cells as the electrochemical potential became more negative between 0.3 V to 0.23 V vs NHE. This was also the potential range of nicotinamide and flavin cofactors used in intracellular and extracellular processes . The luminescence from the cells exposed to Co(II) (0.4 ± 0.1 RLU/CFU) was approximately half the intensity of cells exposed to 0.05 mM nitrate (1.3 ± 0.3 RLU/CFU).…”

“…Many of the bioelectrochemical mechanisms assigned to bacteria that can sense metals and other oxidized compounds will also be sensitive to the electrochemical potentials in their environment . Several biotechnology applications use the redox potential of the medium to manipulate microbial consortia, improve the tolerance of microorganisms to a toxin, or control anaerobic and microaerobic fermentation rates and efficiencies . Control over these electrochemical potentials is essential for the survival of a microorganism on an oxidized metal or compound, and could be one of the reasons why quinones, flavins, and other redox cofactors are secreted by organisms in the first place.…”

A Big World in Small Grain: A Review of Natural Milk Kefir Starters

“…Species, as members of a community, typically influence each other's growth and metabolism in several modes [41]. Interactions can be classified in two groups: (i) Direct, through physical contacts, and (ii) Indirect, either through the excretion of signal molecules (inhibitors/stimulators) or changing environmental growth factors (like pH and gas composition) [42].…”

Interrogating metabolism as an electron flow system

“…Considering this interconnected set of redox reactions can crucially allow us to consider electronic circuits as an analogy to metabolic systems [64] on one hand, and to attempt their manipulation by electrochemical means on the other 65 , 66 , 67 . Indeed, it has been shown that influencing the ratio of key electron shuttles (e.g.…”