Construction of a Recombinant Leuconostoc mesenteroides CJNU 0147 Producing 1,4-Dihydroxy-2-Naphthoic Acid, a Bifidogenic Growth Factor

Eom, Ji-Eun; Moon, Gi-Seong

doi:10.5851/kosfa.2015.35.6.867

Cited by 3 publications

(2 citation statements)

References 29 publications

(31 reference statements)

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“…In food fermentations, L. plantarum is frequently found together with LAB known to synthesize quinones (Eom and Moon, 2015; Mevers et al, 2019; Morishita et al, 1999). To determine whether the secreted products from those LAB influence L. plantarum EET activity, we measured ferrihydrite reduction by L. plantarum during incubation in cell-free, spent-medium (CFS) collected after growth of the quinone-producer L. lactis TIL46 and a quinone-deficient, menC deletion mutant of that strain, TIL999 (Tachon et al, 2010) ( Supplementary Figure S4A ).…”

Section: Resultsmentioning

confidence: 99%

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Lactiplantibacillus plantarumuses ecologically relevant, exogenous quinones for extracellular electron transfer

Stevens

Beeck

Blackburn

et al. 2023

Preprint

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Extracellular 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 by Lactiplantibacillus plantarum, a microorganism required for food fermentations, performs EET, and is also a quinone auxotroph. L. plantarum selectively 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 inhibited L. plantarum growth in non-aerated conditions. Transcriptomic analysis showed that DHNA induced oxidative stress in L. plantarum and 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 induced L. plantarum EET metabolism, although activity was still dependent on the presence of exogenous electron shuttles. To determine whether quinone-producing bacteria frequently found together with L. plantarum in food fermentations could be a source of those electron shuttles, L. plantarum EET was measured after incubation with Lactococcus lactis and Leuconostoc mesenteroides. Quinone-producing L. lactis, but not a quinone-deficient L. lactis ΔmenC mutant, increased L. plantarum ferrihydrite reduction and medium acidification through an EET-dependent mechanism. L. plantarum EET was also stimulated by L. mesenteroides, and this resulted in greater environmental acidification and transient increases in L. plantarum growth. Overall, our findings revealed that L. plantarum overcomes 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.

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Section: Resultsmentioning

confidence: 99%

“…To this regard, extracellular ACNQ was found in spent media from L. lactis (Mevers et al, 2019). Other LAB genera including Leuconostoc, Weissella, and Enterococcus are also capable of synthesizing DHNA (Eom and Moon, 2015) or menaquinones (Pedersen et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

Lactiplantibacillus plantarumuses ecologically relevant, exogenous quinones for extracellular electron transfer

Stevens

Beeck

Blackburn

et al. 2023

Preprint

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Lactiplantibacillus plantarum uses ecologically relevant, exogenous quinones for extracellular electron transfer

Stevens,

Van Beeck,

Blackburn

et al. 2023

mBio

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Extracellular 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 capable of EET but unable to synthesize their own quinones remains to be determined. To address this question, we investigated quinone utilization by Lactiplantibacillus plantarum , a microorganism required for food fermentations, that performs EET and is also a quinone auxotroph. L. plantarum selectively used 1,4-dihydroxy-2-naphthoic acid (DHNA) and more hydrophilic naphthoquinones for EET reduction of insoluble iron (ferrihydrite). However, quinones used for EET also inhibited L. plantarum growth in non-aerated conditions. Transcriptomic analysis showed that DHNA-induced oxidative stress in L. plantarum, but this was alleviated when the electron acceptor, ferric ammonium citrate (FeAC), was included in the growth medium. Although DHNA and FeAC induced L. plantarum EET, this metabolism was still dependent on direct access to environmental electron shuttles. To determine whether quinone-producing food fermentation bacteria could be sources of those electron shuttles, L. plantarum EET was measured after incubation with Lactococcus lactis and Leuconostoc mesenteroides . Quinone-producing L. lactis , but not a quinone-deficient L. lactis Δ menC mutant, increased L. plantarum ferrihydrite reduction and medium acidification through an EET-dependent mechanism. L. plantarum EET was also stimulated by L. mesenteroides , resulting in greater environmental acidification and transient increases in L. plantarum cell numbers. Our findings show that L. plantarum overcomes the toxic effects of exogenous quinones to use those compounds for EET-conferred, ecological advantages during the early stages of food fermentations. IMPORTANCE While quinones are essential for respiratory microorganisms, their importance for microbes that rely on fermentation metabolism is not understood. This gap in knowledge hinders our understanding of anaerobic microbial habitats, such in mammalian digestive tracts and fermented foods. We show that Lactiplantibacillus plantarum, a model fermentative lactic acid bacteria species abundant in human, animal, and insect microbiomes and fermented foods, uses multiple exogenous, environmental quinones as electron shuttles for a hybrid metabolism involving EET. Interestingly, quinones both stimulate this metabolism as well as cause oxidative stress when extracellular electron acceptors are absent. We also found that quinone-producing, lactic acid bacteria species commonly enriched together with L. plantarum in food fermentations accelerate L. plantarum growth and medium acidification through a mainly quinone- and EET-dependent mechanism. Thus, our work provides evidence of quinone cross-feeding as a key ecological feature of anaerobic microbial habitats.

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Isolation and Characterization of Bifidobacterium Growth Stimulator Produced by Leuconostoc mesenteroides isolated from Kimchi

Kwon,

Park

2023

Resour Sci Res

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Genus Bifidobacterium is known to be beneficial gut bacteria, and some strains of Bifidobacterium are being used as probiotics. To find lactic acid bacteria (LAB) that produce Bifidobacterium growth stimulator (BGS), which promotes the growth of Bifidobacterium, we used 733 strains isolated from kimchi for BGS screening and selected strain K748, which showed the highest BGS activity at 320 AU/mL. The strain was identified as Leuconostoc mesenteroides by 16s rDNA sequencing, and the strain was named L. mesenteroides K748. BGS activity increased from 12 hours after incubation in MRS medium, reaching maximum activity (320 AU/mL) at 15 hours and maintaining that activity. The ethyl acetate extract of L. mesenteroides K748 culture supernatant promoted the growth of Bifidobacterium longum, and HPLC using this extract revealed a peak with the same retention time (7.5 minutes) as 1,4-dihydroxy-2-naphthoic acid (DHNA). LC-MS analysis revealed that the DHNA and ethyl acetate extracts of L. mesenteroides K748 had the same molecular weight, 204.1. Overall, it is possible to conclude that L. mesenteroides K748 produces DHNA that promotes the growth of Bifidobacterium.

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Construction of a Recombinant Leuconostoc mesenteroides CJNU 0147 Producing 1,4-Dihydroxy-2-Naphthoic Acid, a Bifidogenic Growth Factor

Cited by 3 publications

References 29 publications

Lactiplantibacillus plantarumuses ecologically relevant, exogenous quinones for extracellular electron transfer

Lactiplantibacillus plantarumuses ecologically relevant, exogenous quinones for extracellular electron transfer

Lactiplantibacillus plantarum uses ecologically relevant, exogenous quinones for extracellular electron transfer

Isolation and Characterization of Bifidobacterium Growth Stimulator Produced by Leuconostoc mesenteroides isolated from Kimchi

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