Electrons from Solid Electrode Alter Phototrophic Mat Morphology and Metabolic Activity
Authors: Ha Phuc Thi , Renslow Ryan Scott , Atci Erhan , Reardon Patrick N. , Lindemann Stephen , Fredrickson James , Call Douglas , Beyenal Haluk 
Published: February 2020

Phototrophic microbial mats are structured microbial communities composed of highly interactive species that have complete energy and elements within them. Aside from being an excellent ecological model that can be used to investigate how microbial populations associate and interact, microbial mats have the potential for energy capture and conversion applications. To use mats for such purpose, it is critical to understand the energy transfer and activity of microbial populations under the existence of external electron donor or acceptor sources. One method to accomplish this is by introducing a solid electrode with a controlled electrochemical potential to act as an electron donor or acceptor to the mat systems. We hypothesized that varying the electrode potential would, in turn, change the structure, activity, and community composition of the mat via regulation of electron transfer processes. In this work, the electrodes were placed under mats to establish a mat electrochemical system for testing our hypothesis. The phototrophic microbial mat was harvested from Hot Lake, a hypersaline, epsomitic lake located near Oroville (Washington, USA). The electrodes in contact with the base of the mat were polarized at -0.7 VAg/AgCl (hereafter referred to as the “cathodic mat)”. Electrodes that served as an electron sink were polarized at +0.3 VAg/AgCl (hereafter referred as the “anodic mat”). We quantified the diel variations of electron transfer rates between the electrode and the cathodic or anodic mats. We observed variations in current over a diel light cycle in which the lowest and highest magnitudes of anodic current occurred simultaneously with those of cathodic current. To understand the factors affecting these variations we examined the influences of temperature, light intensity, and substrate additions, separately, to electron transfer rate. We also used microelectrodes to measure the depth profiles of sulfide and oxygen concentrations and compared them with the variations of electron transfer rates over a diel cycle. To understand how anodic or cathodic electron transfer processes impacted mat structure and activity, we used nuclear magnetic resonance (NMR) imaging for morphology and NMR metabolite analysis to quantify the activity. The results showed that the quantitative porosity and diffusion coefficients were higher in the cathodic mat than in the anodic mat. In addition, cathodic mats produced significantly higher concentrations of osmo-protectants such as betaine and trehalose. The anodic mat had metabolic profiles similar to the control (non-polarized) mat. Finally, we employed amplicon sequencing across the V4 region of the 16S gene to determine the effect of the electrochemical regime upon mat community structure. The community structure data were consistent with variations in metabolite profiles and suggested greater changes in microbial community structure and function in the cathodic vs. the anodic and control mats. Although further work is needed to determine whether the electron transfer to and from the electrode to the mat was mediated by microbial metabolism of selectively-enriched community on the electrode or was caused by abiotic reactions on electrode, our data strongly suggest that donation of electrons via a solid electrode is capable of altering phototrophic mat morphology, community composition, and metabolic activity. It is possible that the addition of electrons from electrode to the mat alleviated the energy limitations allowing the mat to maintain large carbon pools of osmolytes. In addition, some microorganisms in the mat might use electrons from the electrode to drive carbon fixations which resulted in selectively-enriched community on the electrode and the increase of the total carbon available to the mat.