A secondary metabolite drives intraspecies antagonism in a gut symbiont that is inhibited by cell-wall acetylation

Özçam, Mustafa; Oh, Jee-Hwan; Tocmo, Restituto; Acharya, Deepa; Zhang, Shenwei; Astmann, Theresa J; Heggen, Mark; Ruiz-Ramírez, Silvette; Li, Fuyong; Cheng, Chu; Vivas, Eugenio I.; Rey, Federico E.; Claesen, Jan; Bugni, Tim S.; Walter, Jens; Pijkeren, Jan-Peter van

doi:10.1016/j.chom.2022.03.033

Cited by 14 publications

(8 citation statements)

References 66 publications

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“…This is especially valid with regard to microorganisms inhabiting food products, FMPs in particular. Secondary metabolites are often synthesized by means of special enzyme machinery, usually encoded by biosynthetic gene clusters [ 87 ]. Altogether, 392 clusters involved in the biosynthesis of 28 bioactive compound types were found in the studied metagenomes ( Figure 4 ).…”

Section: Resultsmentioning

confidence: 99%

“…For a long time, no aryl polyenes biosynthesis genes had been found in the genomes of lactic acid bacteria [ 89 ]. Recently, it was shown that a mammalian gut inhabitant, Limosilactobacillus reuteri , also involved in food fermentation [ 90 ], produced polyene-like compounds that lysed competitor strains [ 87 ]. This may suggest an antimicrobial function of these substances in microbial communities inhabiting the analyzed products.…”

Section: Resultsmentioning

confidence: 99%

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Metagenomic Insights into the Taxonomic and Functional Features of Traditional Fermented Milk Products from Russia

Elcheninov,

Zayulina,

Klyukina

et al. 2023

Microorganisms

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Fermented milk products (FMPs) contain probiotics that are live bacteria considered to be beneficial to human health due to the production of various bioactive molecules. In this study, nine artisanal FMPs (kefir, ayran, khurunga, shubat, two cottage cheeses, bryndza, khuruud and suluguni-like cheese) from different regions of Russia were characterized using metagenomics. A metagenomic sequencing of ayran, khurunga, shubat, khuruud and suluguni-like cheese was performed for the first time. The taxonomic profiling of metagenomic reads revealed that Lactococcus species, such as Lc. lactis and Lc. cremoris prevailed in khuruud, bryndza, one sample of cottage cheese and khurunga. The latter one together with suluguni-like cheese microbiome was dominated by bacteria, affiliated to Lactobacillus helveticus (32–35%). In addition, a high proportion of sequences belonging to the genera Lactobacillus, Lactococcus and Streptococcus but not classified at the species level were found in the suluguni-like cheese. Lactobacillus delbrueckii, as well as Streptococcus thermophilus constituted the majority in another cottage cheese, kefir and ayran metagenomes. The microbiome of shubat, produced from camel’s milk, was significantly distinctive, and Lentilactobacillus kefiri, Lactobacillus kefiranofaciens and Bifidobacterium mongoliense represented the dominant components (42, 7.4 and 5.6%, respectively). In total, 78 metagenome-assembled genomes with a completeness ≥ 50.2% and a contamination ≤ 8.5% were recovered: 61 genomes were assigned to the Enterococcaceae, Lactobacillaceae and Streptococcaceae families (the Lactobacillales order within Firmicutes), 4 to Bifidobacteriaceae (the Actinobacteriota phylum) and 2 to Acetobacteraceae (the Proteobacteria phylum). A metagenomic analysis revealed numerous genes, from 161 to 1301 in different products, encoding glycoside hydrolases and glycosyltransferases predicted to participate in lactose, alpha-glucans and peptidoglycan hydrolysis as well as exopolysaccharides synthesis. A large number of secondary metabolite biosynthetic gene clusters, such as lanthipeptides, unclassified bacteriocins, nonribosomal peptides and polyketide synthases were also detected. Finally, the genes involved in the synthesis of bioactive compounds like β-lactones, terpenes and furans, nontypical for fermented milk products, were also found. The metagenomes of kefir, ayran and shubat was shown to contain either no or a very low count of antibiotic resistance genes. Altogether, our results show that traditional indigenous fermented products are a promising source of novel probiotic bacteria with beneficial properties for medical and food industries.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Metagenomic Insights into the Taxonomic and Functional Features of Traditional Fermented Milk Products from Russia

Elcheninov,

Zayulina,

Klyukina

et al. 2023

Microorganisms

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“…Additionally, L. reuteri PKS was recently demonstrated to exhibit antimicrobial activity and to drive interspecies antagonism 15 . Yet, the vast majority of microbiota encoded PKS are of unknown function and mechanistic studies linking specific microbial natural products to host phenotypes are scarce.…”

Section: Introductionmentioning

confidence: 99%

“…A PKS cluster of the rodent gut symbiont Limosilactobacillus reuteri is required for activating the mammalian aryl hydrocarbon receptor (AhR), which is involved in mucosal immunity 14 . Additionally, L. reuteri PKS was recently demonstrated to exhibit antimicrobial activity and to drive interspecies antagonism 15 . Yet, the vast majority of microbiota encoded PKS are of unknown function and mechanistic studies linking specific microbial natural products to host phenotypes are scarce.…”

Section: Introductionmentioning

confidence: 99%

Polyketide synthase-derived sphingolipids determine microbiota-mediated protection against pathogens inC. elegans

Peters,

Drechsler,

Pees

et al. 2024

Preprint

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Protection against pathogens is a major function of the gut microbiota. Although bacterial natural products have emerged as crucial components of host-microbiota interactions, their exact role in microbiota-mediated protection is largely unexplored. We addressed this knowledge gap with the nematode Caenorhabditis elegans and its microbiota isolate Pseudomonas fluorescens MYb115 that is known to protect against Bacillus thuringiensis (Bt) infection. We find that MYb115-mediated protection depends on sphingolipids that are derived from an iterative type I polyketide synthase (PKS), thereby describing a noncanonical pathway of bacterial sphingolipid production. We provide evidence that MYb115-derived sphingolipids affect C. elegans tolerance to Bt infection by altering host sphingolipid metabolism. This work establishes sphingolipids as structural outputs of bacterial PKS and highlights the role of microbiota-derived sphingolipids in host protection against pathogens.

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“…For example, L. reuteri converts glycerol into a spectrum of antimicrobial compounds, e.g., reuterin, which suppresses the growth of pathogens and other microorganisms ( 34 ). Importantly, L. reuteri R2lc also produces other antimicrobial metabolites, such as polyketides, and activates aryl hydrocarbon receptor (AhR), which is associated with intestinal inflammation ( 35 , 36 ). Lactobacillus gasseri protects the intestine from dextran sodium sulfate (DSS)-induced colitis and maintains immune homeostasis by increasing the antioxidant response ( 37 ).…”

Section: Introductionmentioning

confidence: 99%

Probiotic Consortia and Their Metabolites Ameliorate the Symptoms of Inflammatory Bowel Diseases in a Colitis Mouse Model

Liu

Huang

et al. 2022

Microbiol Spectr

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A secondary metabolite drives intraspecies antagonism in a gut symbiont that is inhibited by cell-wall acetylation

Cited by 14 publications

References 66 publications

Metagenomic Insights into the Taxonomic and Functional Features of Traditional Fermented Milk Products from Russia

Metagenomic Insights into the Taxonomic and Functional Features of Traditional Fermented Milk Products from Russia

Polyketide synthase-derived sphingolipids determine microbiota-mediated protection against pathogens inC. elegans

Probiotic Consortia and Their Metabolites Ameliorate the Symptoms of Inflammatory Bowel Diseases in a Colitis Mouse Model

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