Energetic Limitations on Microbial Respiration of Organic Compounds using Aqueous Fe(III) Complexes

Abstract:

Soil organic matter constitutes up to 75% of the terrestrial carbon stock. Microorganisms mediate the breakdown of organic compounds and the return of carbon to the atmosphere, predominantly through respiration. Microbial respiration requires an electron acceptor and an electron donor such as small fatty acids, organic acids, alcohols, sugars, and other molecules that differ in oxidation state of carbon. Carbon redox state affects how much energy is required to oxidize a molecule through respiration. Therefore, different organic compounds should offer a spectrum of energies to respiring microorganisms.

However, microbial respiration has traditionally focused on the availability and reduction potential of electron acceptors, ignoring the organic electron donor. We found through incubation experiments that the organic compound serving as electron donor determined how rapidly Shewanella putrefaciens CN32 respires organic substrate and the extent of reduction of the electron acceptor. We simulated a range of energetically favorable to unfavorable electron acceptors using organic chelators bound to Fe(III) with equilibrium stability constants ranging from log(K) of 11.5 to 25.0 for the 1:1 complex, where more stable complexes are less favorable for microbial respiration. Organic substrates varied in nominal oxidation state of carbon from +2 to -2. The most energetically favorable substrate, lactate, promoted up to 30x more rapid increase in percent Fe(II) compared to less favorable substrates such as formate. This increased respiration on lactate was more substantial with less stable Fe(III)-chelate complexes. Intriguingly, this pattern contradicts respiration rate predicted by nominal oxidation state of carbon.

Our results suggest that organic substrates will be consumed so long as the energetic toll corresponding to the electron donor half reaction is counterbalanced by the energy available from the electron accepting half reaction. We propose using the chemical structure of organic matter, elucidated with techniques such as FT-ICR MS, to improve microbial decomposition and carbon cycling models by incorporating energetic limitations due to carbon oxidation.