Abstract
Lactococcus cremoris and L. lactis are well known for their occurrence and applications in dairy fermentations, but their niche extends to a range of natural and food production environments. L. cremoris and L. lactis produce MKs (vitamin K2), mainly as the long-chain forms represented by MK-9 and MK-8, and a detectable number of short-chain forms represented by MK-3. The physiological significance of the different MK forms in the lifestyle of these bacterial species has not been investigated extensively. In this study, we used L. cremoris MG1363 to construct mutants producing different MK profiles by deletion of genes encoding (i) a menaquinone-specific isochorismate synthase, (ii) a geranyltranstransferase, and (iii) a prenyl diphosphate synthase. These gene deletions resulted in (i) a non-MK producer (ΔmenF), (ii) a presumed MK-1 producer (ΔispA), and (iii) an MK-3 producer (Δllmg_0196), respectively. By examining the phenotypes of the MG1363 wildtype strain and respective mutants, including biomass accumulation, stationary phase survival, oxygen consumption, primary metabolites, azo dye/copper reduction, and proteomes, under aerobic, anaerobic, and respiration-permissive conditions, we could infer that short-chain MKs like MK-1 and MK-3 are preferred to mediate extracellular electron transfer and reaction with extracellular oxygen, while the long-chain MKs like MK-9 and MK-8 are more efficient in aerobic respiratory electron transport chain. The different electron transfer routes mediated by short-chain and long-chain MKs likely support growth and survival of L. cremoris in a range of (transiently) anaerobic and aerobic niches including food fermentations, highlighting the physiological significance of diverse MKs in L. cremoris.
Highlights
Lactococcus cremoris [previous known as Lactococcus lactis ssp. cremoris (Li et al, 2021)] and L. lactis are lactic acid bacteria (LAB) that play important roles in food fermentation processes, especially in the manufacturing of fermented dairy products: they are the main constituent of various dairy starter cultures used all over the world for the production of cheese, buttermilk, and sour cream (Cavanagh et al, 2015)
L. cremoris is classified as a facultative anaerobe with a fermentative metabolism, evidence has been provided that in presence of oxygen and exogenous supplemented of heme, the organism can switch to aerobic respiration, a process enabled by the menaquinones (MKs, referred to as vitamin K2) produced by L. cremoris as electron carriers (Duwat et al, 2001; Brooijmans et al, 2009c)
The MK biosynthesis pathway in L. cremoris MG1363 was predicted based on information retrieved from KEGG (Kanehisa and Goto, 2000) and the genome of L. cremoris MG1363 (Wegmann et al, 2007) and homology searches based on sequences from other bacteria with experimentally confirmed functions (Figure 1)
Summary
Lactococcus cremoris [previous known as Lactococcus lactis ssp. cremoris (Li et al, 2021)] and L. lactis are lactic acid bacteria (LAB) that play important roles in food fermentation processes, especially in the manufacturing of fermented dairy products: they are the main constituent of various dairy starter cultures used all over the world for the production of cheese, buttermilk, and sour cream (Cavanagh et al, 2015). Roles of Menaquinones in Lactococcus fermentation of food raw materials highlights the interest in understanding the physiology and lifestyle of this bacterium. L. cremoris and L. lactis are best known for their application and occurrence in dairy products, they are found in a diverse range of natural niches such as the gastrointestinal tract of particular fish species and various plant materials (Cavanagh et al, 2015). Many other LAB species commonly applied in food fermentation processes, e.g., Lactiplantibacillus plantarum [previously referred to as Lactobacillus plantarum (Zheng et al, 2020)], have lost the ability to produce MKs (Pedersen et al, 2012). The ecological and physiological significance of MKs and their contribution to the successful applications of L. cremoris in food fermentations is an interesting, but under-explored topic
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