NoxE NADH Oxidase and the Electron Transport Chain Are Responsible for the Ability of Lactococcus lactis To Decrease the Redox Potential of Milk

Abstract

The redox potential plays a major role in the microbial and sensorial quality of fermented dairy products. The redox potential of milk (around 400 mV) is mainly due to the presence of oxygen and many other oxidizing compounds. Lactococcus lactis has a strong ability to decrease the redox potential of milk to a negative value (؊220 mV), but the molecular mechanisms of milk reduction have never been addressed. In this study, we investigated the impact of inactivation of genes encoding NADH oxidases (noxE and ahpF) and components of the electron transport chain (ETC) (menC and noxAB) on the ability of L. lactis to decrease the redox potential of ultrahigh-temperature (UHT) skim milk during growth under aerobic and anaerobic conditions. Our results revealed that elimination of oxygen is required for milk reduction and that NoxE is mainly responsible for the rapid removal of oxygen from milk before the exponential growth phase. The ETC also contributes slightly to oxygen consumption, especially during the stationary growth phase. We also demonstrated that the ETC is responsible for the decrease in the milk redox potential from 300 mV to ؊220 mV when the oxygen concentration reaches zero or under anaerobic conditions. This suggests that the ETC is responsible for the reduction of oxidizing compounds other than oxygen. Moreover, we found great diversity in the reducing activities of natural L. lactis strains originating from the dairy environment. This diversity allows selection of specific strains that can be used to modulate the redox potential of fermented dairy products to optimize their microbial and sensorial qualities.

Contribution of bacteria to redox potential (E h) measurements in sediments

“…This corroborates redox development described for other bacterial species (e.g. Brasca et al 2007;Reichart et al 2007;Tachon et al 2010). At the onset of the stationary growth phase, redox potential measurements became more variable.…”

“…These include membrane bound pili, cytochromes and electron transport systems, and also the secretion of electron transport system related redox mediators such as cytochrome b/c, flavins and quinones in the extracellular matrix that either remain soluble or bind to electrodes (e.g. Rabaey et al 2007;Lovley 2008;Marsili et al 2008;Tachon et al 2010;Juang et al 2011). These compounds are produced in order to dispose respiratory electrons in the absence of terminal electron acceptors in the immediate environment, allowing electron shuttling to distant terminal electron acceptors (Rabaey et al 2007;Xie et al 2010).…”

“…Increasing evidence suggests that bacteria are capable of creating redox conditions which are visible as speciesspecific continuous E h measurements (Brasca et al 2007;Reichart et al 2007;Michelon et al 2010;Ignatova et al 2010;Tachon et al 2010). It has been demonstrated that continuous measurements of E h are valuable for tracking bacterial metabolic activities in liquid cultures (e.g.…”

Non-enzymic copper reduction by menaquinone enhances copper toxicity in Lactococcus lactis IL1403

“…Thus, any opportunity to pass electrons on to a substrate will be favourable for the cells. It has been shown that menaquinones contribute substantially to the reduction of the redox potential of milk by L. lactis (Tachon et al, 2010). Copper appears to also be a suitable acceptor for excess reducing equivalents, resulting in the observed extracellular copper reductase activity.…”

“…In milk, where L. lactis most often grows, it substantially reduces the redox potential of the milk, presumably as a way of disposing of excess reducing equivalents (Tachon et al, 2010). Fig.…”