Microbial manganese(III) reduction fuelled by anaerobic acetate oxidation

Abstract

Soluble manganese in the intermediate +III oxidation state (Mn ) is a newly identified oxidant in anoxic environments, whereas acetate is a naturally abundant substrate that fuels microbial activity. Microbial populations coupling anaerobic acetate oxidation to Mn reduction, however, have yet to be identified. We isolated a Shewanella strain capable of oxidizing acetate anaerobically with Mn as the electron acceptor, and confirmed this phenotype in other strains. This metabolic connection between acetate and soluble Mn represents a new biogeochemical link between carbon and manganese cycles. Genomic analyses uncovered four distinct genes that allow for pathway variations in the complete dehydrogenase-driven TCA cycle that could support anaerobic acetate oxidation coupled to metal reduction in Shewanella and other Gammaproteobacteria. An oxygen-tolerant TCA cycle supporting anaerobic manganese reduction is thus a new connection in the manganese-driven carbon cycle, and a new variable for models that use manganese as a proxy to infer oxygenation events on early Earth.

Oxidation of Mn(III) Species by Pb(IV) Oxide as a Surrogate Oxidant in Aquatic Systems

“…A holistic understanding of the environmental geochemistry of dissolved Mn­(III) complexes includes the aqueous complexation and electron transfer (redox) processes. A number of studies have established the fundamentals of Mn­(III)–ligand complexation affinity and the significant role of dissolved Mn­(III) as a potent oxidant in subsurface geochemical processes, − surface water photochemical processes, − and advanced oxidation processes. − In these contexts, dissolved Mn­(III) complexes were usually regarded as reactive intermediates that could accept an additional electron to reduce themselves to dissolved Mn­(II), thereby oxidizing other reactants such as reduced metals and organic compounds. Nevertheless, very little is known regarding the role of dissolved Mn­(III) complexes as a reductant in environmentally relevant water chemistry conditions.…”

<i>Shewanella algae</i> Relatives Capable of Generating Electricity from Acetate Contribute to Coastal-Sediment Microbial Fuel Cells Treating Complex Organic Matter

“…Therefore, catabolic pathways in S. algae strains differ from those in authentic Shewanella strains, including strain MR-1, and it will be interesting to investigate their catabolic pathways. A recent study demonstrated that a novel isolate of S. algae exhibited the ability to oxidize acetate with manganese(III) as the sole electron acceptor (Szeinbaum et al, 2017). Therefore, acetate oxidation under anaerobic conditions may be a common feature of S. algae strains that is distinct from other Shewanella strains.…”

Understanding and engineering electrochemically active bacteria for sustainable biotechnology

“…In contrast, other EAB, including Geobacter spp. and Shewanella algae, are able to oxidize acetate to CO 2 coupled to metal respiration, since the complete TCA cycle is operational in these bacteria even under anaerobic conditions (Bond and Lovley 2003;Szeinbaum et al 2017).…”