Lactiplantibacillus plantarumuses ecologically relevant, exogenous quinones for extracellular electron transfer

Abstract

AbstractExtracellular electron transfer (EET) is a metabolic process that frequently uses quinones to couple intracellular redox reactions with extracellular electron acceptors. The physiological relevance of this metabolism for microorganisms that are capable of EET, but unable to synthesize their own quinones, remains to be determined. To address this question, we investigated quinone utilization byLactiplantibacillus plantarum,a microorganism required for food fermentations, performs EET, and is also a quinone auxotroph. L. plantarumselectively used 1,4-dihydroxy-2-naphthoic acid (DHNA), 2-amino-3-carboxy-1,4-naphthoquinone (ACNQ), 1,4-naphthoquinone, and menadione for EET reduction of insoluble iron (ferrihydrite). However, those quinones used for EET also inhibitedL. plantarumgrowth in non-aerated conditions. Transcriptomic analysis showed that DHNA induced oxidative stress inL. plantarumand this was alleviated by the inclusion of an electron acceptor, soluble ferric ammonium citrate (FeAC), in the laboratory culture medium. The presence of DHNA and FeAC during growth also inducedL. plantarumEET metabolism, although activity was still dependent on the presence of exogenous electron shuttles. To determine whether quinone-producing bacteria frequently found together withL. plantarumin food fermentations could be a source of those electron shuttles,L. plantarumEET was measured after incubation withLactococcus lactisandLeuconostoc mesenteroides.Quinone-producingL. lactis,but not a quinone-deficientL. lactisΔmenCmutant, increasedL. plantarumferrihydrite reduction and medium acidification through an EET-dependent mechanism.L. plantarumEET was also stimulated byL. mesenteroides, and this resulted in greater environmental acidification and transient increases inL. plantarumgrowth. Overall, our findings revealed thatL. plantarumovercomes the toxic effects of exogenous quinones to use those compounds, including those made by related bacteria, for EET-conferred, ecological advantages during the early stages of food fermentations.