Investigation of the primary mechanism for entropy export of metal-reducing microorganisms

Introduction
Two fundamental principles of life are coupling electron donor oxidation with electron acceptor reduction for energy harvest and exporting entropy into the environment by secretion of small molecules or heat dissipation. Chemotrophic microorganisms evolved to exploit numerous combinations of electron donor and acceptor, resulting in different mechanisms for entropy export ranging from purely entropy-driven to enthalpy-driven growth^[1]. Metal-reducing microorganisms represent a unique variation as they couple their metabolism with insoluble electron acceptors by performing extracellular electron transfer (EET). This process allows the microbes to exchange metabolic electrons with metal ores in nature or electrodes in technical systems. Electrons undergo a phase shift from the liquid to the solid state during EET. Thus, the entropy export of metal-reducing microbes is supposed to differ from microbes utilizing soluble electron acceptors that has energetic consequences for the metabolism.

Goal
Analysis of the entropy export of metal-reducing microorganisms performing EET.

Materials&Methods
A bioelectrocalorimetric setup was employed to measure the heat flux of Geobacter sulfurreducens and Geobacter enrichment biofilms during EET with different electrode materials. Furthermore, the contribution of the electrolyte to the heat flux was assessed by applying the entropy of transport concept and fundamental equations^[2]. The electrodes were microscopically and spectroscopically analyzed to elucidate the impact of EET on the elemental composition of the electrodes and to visualize biofilm formation.

Results
We show that the heat evolution depends on the electrode material amounting to 27.3±4.7, 22.1±4.5, and 13.2±5.0 kJ e-mol⁻¹ for Geobacter enrichment biofilms at silver, copper, and gold electrodes. For G. sulfurreducens at graphite electrodes, 27.2±8.1 kJ e-mol⁻¹ were measured, validating first experiments^[3]. It is shown that Geobacter"s entropy export differs from microorganisms utilizing soluble electron acceptors as it mainly relies on EET and not the secretion of small molecules or dissipation of heat.

Summary
Bioelectrocalorimetric experiments show that electron transfer facilitates the main share of entropy export for metal-reducing microbes and depends on the electron acceptor material.

References
[1] von Stockar, U., et al. 1999. Biochim. Biophys. Acta. 1412
[2] Agar, J.N. 1963. Thermogalvanic Cells
[3] Korth, B., et al. 2016. Energy Environ. Sci. 9