Modelling of mechanical and electrochemical interspecies interactions in microbial communities

Abstract

Microbial interactions play an important role in environmental processes, both beneficial (e.g., production of methane through anaerobic digestion) and detrimental (e.g., bulking of sludge). By better understanding microbial interactions, conditions can be optimised to either make the microbial processes more effective or limit the negative effects caused by the microbial community. This thesis mathematically investigates physical and chemical microbial interspecies interactions in order to determine the impact of elementary controlling mechanisms. Research is focused on basic mechanical interactions and chemical-electrochemical interspecies interactions, with application to key systems where the physical, electrical, and chemical elements are linked. To enable description of the physical components, an extendible individual-based modelling framework is presented that predicts the movement, growth and development of single cells, as well as their interactions with surfaces and other cells in the microbial community (chapter 2). This extends previous approaches to consider physics at the level of individual cells and enables the use of non-spherical cell geometries. Using this model it is shown that (i) in a biofilm consisting of rod-shaped cells, inclusion of cell-substratum anchoring links cause biofilms to rapidly grow in thickness instead of surface area, and (ii) interfloc bridging in activated sludge is related to the relative growth rates of floc forming and filament forming microorganisms. A microbial community where direct interspecies electron transfer occurs is evaluated by modelling both the physical organisation of cells and interspecies links, along with diffusion-migration transport, electrochemistry and biochemical reactions. This allows comparison of the external limitations of a recently reported direct interspecies electron transfer (IET) mechanism to classical, mediated IET through formate or hydrogen (chapter 3). This work shows that direct IET through nanowires is more strongly limited by thermodynamics than formate-mediated IET. Redox complex activation losses encountered during cell-nanowire transfer govern the system (93% of total losses). A sensitivity analysis shows that only when the redox complex transfer rate is an order of magnitude higher or the redox complex count is five times higher does nanowire resistance play a role, yet the feasibility of direct IET remains lower than formate-mediated IET. However, a minor metabolic advantage, as reported in recent literature, is sufficient to explain why direct IET can outcompete formate-mediated IET in some systems despite the limitations governing electron transfer. The techniques developed in chapter 2, as well as reaction-diffusion as applied in chapter 3 are further developed to consider the shell-shaped aggregates mediating anaerobic oxidation of methane in deep sea sediments (chapter 4). Extremely low reaction rates, acid dissociation and polysulfide precipitation cause diffusion to be non-limiting even in the largest reported aggregates, which explains why the aggregate continues to grow despite the thermodynamically suboptimal cell organisation. Using cell-cell EPS links and anti-collision as the sole cell-cell interactions, a shell-shaped morphology analogous to that observed in in vitro experiments can be grown from a small microbial inoculum.