Discovery of extracellular electron uptake by the lactic acid bacterium Lactiplantibacillus plantarum

Abstract

Abstract Microorganisms utilize different electron donors and acceptors to gain energy from redox reactions. A subset of microorganisms that perform respiration can endogenously utilize insoluble electron donors, such as Fe(II) or a cathode, in a process called extracellular electron transfer (EET). However, it is unknown whether similar endogenous EET can be performed by primarily fermentative species like lactic acid bacteria. We report for the first time EET from a cathode by Lactiplantibacillus plantarum, a primarily fermentative bacteria found in the gut of mammals and in fermented foods. L. plantarum consumed electrons from a cathode and coupled this oxidation to the reduction of both an endogenous organic and an exogenous inorganic electron acceptor. This EET from a cathode reroutes glucose fermentation towards ATP generation routes and provides cells with a higher viability upon sugar exhaustion. Moreover, the associated genes and cofactors indicate that this pathway is distinct from any other known electron transport chains within the group of lactic acid bacteria. Our results expand our knowledge of the diversity of electroactive species and of the metabolic and bioenergetic strategies used by lactic acid bacteria.