Starvation combined with constant anode potential triggers intracellular electron storage in electro-active biofilms

João Pereira; Patrícia Neves; Vivian Nemanic; Maria Alcina Pereira; Tom Sleutels; Bert Hamelers; Annemiek Ter Heijne

doi:10.1016/j.watres.2023.120278

Starvation combined with constant anode potential triggers intracellular electron storage in electro-active biofilms

Water Res. 2023 Aug 15:242:120278. doi: 10.1016/j.watres.2023.120278. Epub 2023 Jun 27.

Authors

João Pereira¹, Patrícia Neves², Vivian Nemanic³, Maria Alcina Pereira⁴, Tom Sleutels⁵, Bert Hamelers¹, Annemiek Ter Heijne⁶

Affiliations

¹ Wetsus, European Centre of Excellence for Sustainable Water Technology, Oostergoweg 9, 8911 MA, Leeuwarden, the Netherlands; Environmental Technology, Wageningen University, Bornse Weilanden 9, P.O. Box 17, 6700 AA, Wageningen, the Netherlands.
² Wetsus, European Centre of Excellence for Sustainable Water Technology, Oostergoweg 9, 8911 MA, Leeuwarden, the Netherlands; Centre of Biological Engineering, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal.
³ Wetsus, European Centre of Excellence for Sustainable Water Technology, Oostergoweg 9, 8911 MA, Leeuwarden, the Netherlands.
⁴ Centre of Biological Engineering, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal; LABBELS -Associate Laboratory, Braga/Guimarães, Portugal.
⁵ Wetsus, European Centre of Excellence for Sustainable Water Technology, Oostergoweg 9, 8911 MA, Leeuwarden, the Netherlands; Faculty of Science and Engineering, University of Groningen, Nijenborgh 4, 9747 AG, Groningen, the Netherlands.
⁶ Environmental Technology, Wageningen University, Bornse Weilanden 9, P.O. Box 17, 6700 AA, Wageningen, the Netherlands. Electronic address: annemiek.terheijne@wur.nl.

PMID: 37413745
DOI: 10.1016/j.watres.2023.120278

Abstract

The accumulation of electrons in the form of Extracellular Polymeric Substances (EPS) and poly-hydroxyalkanoates (PHA) has been studied in anaerobic processes by adjusting the access of microorganisms to the electron donor and final electron acceptor. In Bio-electrochemical systems (BESs), intermittent anode potential regimes have also recently been used to study electron storage in anodic electro-active biofilms (EABfs), but the effect of electron donor feeding mode on electron storage has not been explored. Therefore, in this study, the accumulation of electrons in the form of EPS and PHA was studied as a function of the operating conditions. EABfs were grown under both constant and intermittent anode potential regimes and fed with acetate (electron donor) continuously or in batch. Confocal Laser Scanning Microscopy (CLSM) and Fourier-Transform Infrared Spectroscopy (FTIR) were used to assess electron storage. The range of Coulombic efficiencies, from 25 to 82%, and the biomass yields, between 10 and 20%, indicate that storage could have been an alternative electron consuming process. From image processing, a 0.92 pixel ratio of poly-hydroxybutyrate (PHB) and amount of cells was found in the batch fed EABf grown under a constant anode potential. This storage was linked to the presence of living Geobacter and shows that energy gain and carbon source starvation were the triggers for intracellular electron storage. The highest EPS content (extracellular storage) was observed in the continuously fed EABf under an intermittent anode potential, showing that constant access to electron donor and intermittent access to the electron acceptor leads to the formation of EPS from the excess energy gained. Tailoring operating conditions can thus steer the microbial community and result in a trained EABf to perform a desired biological conversion, which can be beneficial for a more efficient and optimized BES.

Keywords: Electro-active biofilms; Electron storage; Feeding modes; Intermittent anode potential.

MeSH terms

Bioelectric Energy Sources*
Biofilms
Electrodes
Electron Transport
Electrons
Extracellular Polymeric Substance Matrix
Geobacter*
Oxidants

Substances

Oxidants