Lactobacillus plantarum WCFS1 Electron Transport Chains

Abstract

Lactobacillus plantarum WCFS1 requires both heme and menaquinone to induce respiration-like behavior under aerobic conditions. The addition of these compounds enhanced both biomass production, without progressive acidification, and the oxygen consumption rate. When both heme and menaquinone were present, L. plantarum WCFS1 was also able to reduce nitrate. The ability to reduce nitrate was severely inhibited by the glucose levels that are typically found in L. plantarum growth media (1 to 2% [vol/vol] glucose). In contrast, comparable mannitol levels did not inhibit the reduction of nitrate. L. plantarum reduced nitrate with concomitant formation of nitrite and ammonia. Genes that encode a bd-type cytochrome (cydABCD) and a nitrate reductase (narGHJI) were identified in the genome of L. plantarum. The narGHJI operon is part of a cluster of genes that includes the molybdopterin cofactor biosynthesis genes and narK. Besides a menaquinone source, isogenic mutants revealed that cydA and ndh1 are required for the aerobic-respiration-like response and narG for nitrate reduction. The ndh1 mutant was still able to reduce nitrate. The existence of a nonredundant branched electron transport chain in L. plantarum WCFS1 that is capable of using oxygen or nitrate as a terminal electron acceptor is proposed.Lactic acid bacteria (LAB) are extensively used for the production of fermented foods from dairy, meat, fruit, and vegetable sources. These fermented foods are valued for their enhanced shelf life, flavor, and structural properties. LAB have been exploited for this purpose for millennia and generally behave as facultative anaerobic, obligate fermentative bacteria.However, the production of cytochromes, typical constituents of respiratory chains, has been observed in several LAB species when they are grown in the presence of heme. These include Lactococcus lactis (Streptococcus lactis), Leuconostoc mesenteroides, and Enterococcus faecalis (36,42).Recently, in L. lactis, generation of a proton motive force by a heme-dependent aerobic electron transport chain was demonstrated (9). In other words, heme induces respiration in L. lactis. L. lactis cells grown under these respiration-permissive conditions have enhanced biomass yields and are more robust (more resistant to oxygen, acid, and cold-storage stress) (15,18,31). Respiration-like behavior has also been reported for Streptococcus agalactiae and Oenococcus oeni (43; A. Gruss, unpublished results). However, there have been no published reports of heme-induced respiration-like behavior in any member of the genus Lactobacillus. This genus contains many species that are used extensively in food fermentation, such as Lactobacillus plantarum.L. plantarum has been isolated from the human gastrointestinal tract and plant surfaces. It is an economically important starter culture bacterium, to initiate food fermentation, and certain strains are even sold as probiotics (2,3,13,40). Improvements in the efficiency of biomass formation and robustness, which are associated with respiratio...

Effect of respiration and manganese on oxidative stress resistance of Lactobacillus plantarum WCFS1

“…plantarum WCFS1 that under specific conditions, i.e. in the presence of haemin and vitamin K 2 , an ETC was active, composed of NADH dehydrogenase, menaquinone (vitamin K 2 ) and cytochrome oxidase, using oxygen as a final electron acceptor (Brooijmans et al, 2009b). Growth of Lb.…”

Respiration, a strategy to avoid oxidative stress in Lactococcus lactis, is regulated by the heme status

“…Lactobacillus plantarum displayed additional respiratory metabolism with nitrate as final electron acceptor. Nitrate respiration also required heme and menaquinone for activity 5) .…”

“…CydC and CydD encode functions implicated in cytochrome oxidase assembly 4,5,16,42) . Once activated, the respiratory chain expulses protons outside the cells, which may then be taken up by the H + -ATPase to produce ATP 3,19) .…”

“…In the last decades, our group or others have identified oxygen-dependant respiratory chain in several LAB indicating that they are better adapted to aerobiosis than we previously thought 4,5,8,16,42,43) .…”

Dynamic Stresses of Lactic Acid Bacteria Associated to Fermentation Processes

“…Respiration-competent LAB differ from the features of Escherichia coli and Bacillus subtilis, since they carry limited equipment for respiration. All respiring LAB carry genes encoding electron donor (NADH dehydrogenase) and a single electron acceptor (cytochrome bd oxidase) [58]. Addition of heme to the system activates respiration chain NADH oxidase activity, but none of the tested LAB synthesize heme [01].…”