PH Dependency in Anode Biofilms of Thermincola ferriacetica Suggests a Proton-Dependent Electrochemical Response

Bradley G. Lusk, Isaias Peraza, Gaurav Albal, Andrew Marcus, Sudeep C. Popat, Cesar Torres

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

Monitoring the electrochemical response of anode respiring bacteria (ARB) helps elucidate the fundamental processes of anode respiration and their rate limitations. Understanding these limitations provides insights on how ARB create the complex interfacing of biochemical metabolic processes with insoluble electron acceptors and electronics. In this study, anode biofilms of the thermophilic (60 °C) Gram-positive ARB Thermincola ferriacetica were studied to determine the presence of a proton-dependent electron transfer response. The effects of pH, the presence of an electron donor (acetate), and biofilm growth were varied to determine their influence on the electrochemical midpoint potential (EKA) and formal redox potential (E°′) under nonturnover conditions. The EKA and E°′ are associated with an enzymatic process within ARB's metabolism that controls the rate and energetic state of their respiration. Results for all conditions indicate that pH was the major contributor to altering the energetics of T. ferriacetica anode biofilms. Electrochemical responses measured in the absence of an electron donor and with a minimal proton gradient within the anode biofilms resulted in a 48 ± 7 mV/pH unit shift in the E°′, suggesting a proton-dependent rate-limiting process. Given the limited energy available for anode respiration (<200 mV when using acetate as electron donor), our results provide a new perspective in understanding proton-transport limitations in ARB biofilms, one in which ARB are thermodynamically limited by pH gradients. Since the anode biofilms of all ARB that perform direct extracellular electron transfer (EET) investigated thus far exhibit an n = 1 Nernstian behavior, and because this behavior is affected by changes in pH, we hypothesize that the Nernstian response is associated with membrane proteins responsible for proton translocation. Finally, this study shows that the EKA and E°′ are a function of pH within the physiological range of ARB, and thus, given the significant effect pH has on this parameter, we recommend reporting the EKA and E°′ of ARB biofilms at a specific bulk pH.

Original languageEnglish (US)
Pages (from-to)5527-5534
Number of pages8
JournalJournal of the American Chemical Society
Volume140
Issue number16
DOIs
StatePublished - Apr 25 2018

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Biofilms
Protons
Anodes
Electrodes
Bacteria
Electrons
Respiration
Acetates
Biochemical Phenomena
pH effects
Proton-Motive Force
Respiratory Rate
Metabolism
Oxidation-Reduction
Membrane Proteins
Electronic equipment

ASJC Scopus subject areas

  • Catalysis
  • Chemistry(all)
  • Biochemistry
  • Colloid and Surface Chemistry

Cite this

PH Dependency in Anode Biofilms of Thermincola ferriacetica Suggests a Proton-Dependent Electrochemical Response. / Lusk, Bradley G.; Peraza, Isaias; Albal, Gaurav; Marcus, Andrew; Popat, Sudeep C.; Torres, Cesar.

In: Journal of the American Chemical Society, Vol. 140, No. 16, 25.04.2018, p. 5527-5534.

Research output: Contribution to journalArticle

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abstract = "Monitoring the electrochemical response of anode respiring bacteria (ARB) helps elucidate the fundamental processes of anode respiration and their rate limitations. Understanding these limitations provides insights on how ARB create the complex interfacing of biochemical metabolic processes with insoluble electron acceptors and electronics. In this study, anode biofilms of the thermophilic (60 °C) Gram-positive ARB Thermincola ferriacetica were studied to determine the presence of a proton-dependent electron transfer response. The effects of pH, the presence of an electron donor (acetate), and biofilm growth were varied to determine their influence on the electrochemical midpoint potential (EKA) and formal redox potential (E°′) under nonturnover conditions. The EKA and E°′ are associated with an enzymatic process within ARB's metabolism that controls the rate and energetic state of their respiration. Results for all conditions indicate that pH was the major contributor to altering the energetics of T. ferriacetica anode biofilms. Electrochemical responses measured in the absence of an electron donor and with a minimal proton gradient within the anode biofilms resulted in a 48 ± 7 mV/pH unit shift in the E°′, suggesting a proton-dependent rate-limiting process. Given the limited energy available for anode respiration (<200 mV when using acetate as electron donor), our results provide a new perspective in understanding proton-transport limitations in ARB biofilms, one in which ARB are thermodynamically limited by pH gradients. Since the anode biofilms of all ARB that perform direct extracellular electron transfer (EET) investigated thus far exhibit an n = 1 Nernstian behavior, and because this behavior is affected by changes in pH, we hypothesize that the Nernstian response is associated with membrane proteins responsible for proton translocation. Finally, this study shows that the EKA and E°′ are a function of pH within the physiological range of ARB, and thus, given the significant effect pH has on this parameter, we recommend reporting the EKA and E°′ of ARB biofilms at a specific bulk pH.",
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