Interfacial extracellular electron uptake is linked to nitrate respiration in the marine heterotroph, Thalassospira xiamenensis SN3

Abstract

Thalassospira species are ubiquitous marine bacteria with poorly understood ecology, and some have been implicated in iron corrosion. To better elucidate the mechanisms and ecological implications of extracellular electron transfer (EET) in oxidative processes, we conducted genomic and bioelectrochemical characterization of Thalassospira xiamenensis strain SN3, an obligate heterotroph isolated from coastal marine sediment cathode-oxidizing enrichments. Physiologic and genomic analyses indicate that SN3 lacks the capacity for lithoautotrophic growth and lacks homologs to genes canonically involved in EET. Bioelectrochemical characterization of SN3 cells shows that inward EET requires a terminal electron acceptor (respiration). Deletion of nitrate reductase catalytic subunit napA abolished current consumption and catalytic activity under nitrate-reducing conditions. Media exchange experiments demonstrate that inward EET in SN3 is facilitated by direct contact with the electrode, with a formal midpoint potential of −153 ± 16 mV vs. SHE. Through deletion of the formate dehydrogenase fdhABCD and electrochemical characterization of mutant cells, we show that inward EET is not a function of Fdh enzyme sorption to the electrode, as has been demonstrated for other organisms. This provides further evidence of a cell-mediated and contact-dependent EET mechanism. This work provides a foundation for investigating this metabolically versatile organism's yet uncharacterized mechanism of EET.