Systematic evaluation of genome-wide metabolic landscapes in lactic acid bacteria reveals diet- and strain-specific probiotic idiosyncrasies

Koduru, Lokanand; Lee, Yi Qing; Ho, Pooi-Leng; Lim, Pei-Yu; Ler, Wei Xuan; Kim, Dongseok; Park, Doo-Sang; Banu, M. Shakeera; Ow, Dave Siak-Wei; Lee, Dong-Yup

doi:10.1016/j.celrep.2022.111735

Cited by 14 publications

(9 citation statements)

References 170 publications

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“…Apart from this they are able to produce a wide range of other metabolites like SCFAs, amines, bacteriocins and vitamins [ 57 ]. They are commonly used as probiotics for intestinal and metabolic health [ 58 ]. Some Lactobacillus taxa were positively, others negatively associated with NASH in our study (Fig.…”

Section: Discussionmentioning

confidence: 99%

Development of non-alcoholic steatohepatitis is associated with gut microbiota but not with oxysterol enzymes CH25H, EBI2, or CYP7B1 in mice

Wyss,

Raselli,

Wyss

et al. 2024

BMC Microbiol

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Liver steatosis is the most frequent liver disorder and its advanced stage, non-alcoholic steatohepatitis (NASH), will soon become the main reason for liver fibrosis and cirrhosis. The “multiple hits hypothesis” suggests that progression from simple steatosis to NASH is triggered by multiple factors including the gut microbiota composition. The Epstein Barr virus induced gene 2 (EBI2) is a receptor for the oxysterol 7a, 25-dihydroxycholesterol synthesized by the enzymes CH25H and CYP7B1. EBI2 and its ligand control activation of immune cells in secondary lymphoid organs and the gut. Here we show a concurrent study of the microbial dysregulation and perturbation of the EBI2 axis in a mice model of NASH.We used mice with wildtype, or littermates with CH25H−/−, EBI2−/−, or CYP7B1−/− genotypes fed with a high-fat diet (HFD) containing high amounts of fat, cholesterol, and fructose for 20 weeks to induce liver steatosis and NASH. Fecal and small intestinal microbiota samples were collected, and microbiota signatures were compared according to genotype and NASH disease state.We found pronounced differences in microbiota composition of mice with HFD developing NASH compared to mice did not developing NASH. In mice with NASH, we identified significantly increased 33 taxa mainly belonging to the Clostridiales order and/ or the family, and significantly decreased 17 taxa. Using an Elastic Net algorithm, we suggest a microbiota signature that predicts NASH in animals with a HFD from the microbiota composition with moderate accuracy (area under the receiver operator characteristics curve = 0.64). In contrast, no microbiota differences regarding the studied genotypes (wildtype vs knock-out CH25H−/−, EBI2−/−, or CYP7B1−/−) were observed.In conclusion, our data confirm previous studies identifying the intestinal microbiota composition as a relevant marker for NASH pathogenesis. Further, no link of the EBI2 – oxysterol axis to the intestinal microbiota was detectable in the current study.

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Section: Discussionmentioning

confidence: 99%

Development of non-alcoholic steatohepatitis is associated with gut microbiota but not with oxysterol enzymes CH25H, EBI2, or CYP7B1 in mice

Wyss,

Raselli,

Wyss

et al. 2024

BMC Microbiol

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“…For instance, C. acnes and Staphylococcus species (e.g., S. epidermidis ), a predominant genus of skin microbiome, have antagonistic relationships by secreting SCFAs that inhibit the growth of each other ( Nakamura et al., 2020 ; Ahle et al., 2022 ). In this regard, model-guided approach can be exploited to understand the roles of C. acnes and S. epidermidis , their relationship and skin community-level metabolic interactions during the development of acne vulgaris as similarly done for lactic acid bacteria strains ( Shoaie et al., 2013 ; Koduru et al., 2022 ) and gut microbiome based on the models derived from AGORA ( Magnúsdóttir et al., 2017 ), thereby providing a springboard for rational design of skin probiotics to restore healthy microbiome or to develop personalized treatment of acne vulgaris in future.…”

Section: Discussionmentioning

confidence: 99%

Genome-scale metabolic modeling and in silico analysis of opportunistic skin pathogen Cutibacterium acnes

Kim

Lee

et al. 2023

Front. Cell. Infect. Microbiol.

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Cutibacterium acnes, one of the most abundant skin microbes found in the sebaceous gland, is known to contribute to the development of acne vulgaris when its strains become imbalanced. The current limitations of acne treatment using antibiotics have caused an urgent need to develop a systematic strategy for selectively targeting C. acnes, which can be achieved by characterizing their cellular behaviors under various skin environments. To this end, we developed a genome-scale metabolic model (GEM) of virulent C. acnes, iCA843, based on the genome information of a relevant strain from ribotype 5 to comprehensively understand the pathogenic traits of C. acnes in the skin environment. We validated the model qualitatively by demonstrating its accuracy prediction of propionate and acetate production patterns, which were consistent with experimental observations. Additionally, we identified unique biosynthetic pathways for short-chain fatty acids in C. acnes compared to other GEMs of acne-inducing skin pathogens. By conducting constraint-based flux analysis under endogenous carbon sources in human skin, we discovered that the Wood-Werkman cycle is highly activated under acnes-associated skin condition for the regeneration of NAD, resulting in enhanced propionate production. Finally, we proposed potential anti-C. acnes targets by using the model-guided systematic framework based on gene essentiality analysis and protein sequence similarity search with abundant skin microbiome taxa.

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“…It has been proven that the metabolic function of LAB differed between species or even strains, which was related to its capacity of growth, intestinal persistence, and biosynthesis. 66,67 Besides, even diet type, gavage dose, treatment duration, and strain status could affect the alleviating effect of LAB on obesity. 68,69 Recently, comparative genomics has been adopted to reveal functional differences between different species or strains, which may provide a new understanding of differences in obesity alleviation by LP, LR, and LF at the genetic level.…”

Section: Discussionmentioning

confidence: 99%

“…The essential difference of this modulation ability on gut microbiota derives from the difference between species or strains. It has been proven that the metabolic function of LAB differed between species or even strains, which was related to its capacity of growth, intestinal persistence, and biosynthesis. , Besides, even diet type, gavage dose, treatment duration, and strain status could affect the alleviating effect of LAB on obesity. , Recently, comparative genomics has been adopted to reveal functional differences between different species or strains, which may provide a new understanding of differences in obesity alleviation by LP, LR, and LF at the genetic level. It was found that the genomes of LAB with weight-reducing functions encoded a large number of glucose permease, which promote sugar degradation rather than conversion to fat for storage in the host.…”

Section: Discussionmentioning

confidence: 99%

Modulation of the Microbiome–Fat–Liver Axis by Lactic Acid Bacteria: A Potential Alleviated Role in High-Fat-Diet-Induced Obese Mice

Wei

Peng

Xiao

et al. 2023

J. Agric. Food Chem.

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The major characteristics of obesity are abnormal lipid metabolism, chronic inflammation, and imbalanced gut microbiota. It has been reported that lactic acid bacteria (LAB) possess potential for alleviating obesity, considering which the strainspecific functions and diverse mechanisms and the roles and mechanisms of various LAB are worthy of investigation. This study aimed to validate and investigate the alleviating effects and underlying mechanisms of three LAB strains, Lactiplantibacillus plantarum NCUH001046 (LP), Limosilactobacillus reuteri NCUH064003, and Limosilactobacillus fermentum NCUH003068 (LF), in high-fatdiet-induced obese mice. The findings demonstrated that the three strains, particularly LP, suppressed body weight gain and fat deposition; ameliorated lipid disorders, liver and adipocyte morphology, and chronic low-grade inflammation; and reduced lipid synthesis via activating the adenosine 5′-monophosphate-activated protein kinase (AMPK) signaling pathway. In addition, LP and LF decreased the enrichment of bacteria positively correlated with obesity, like Mucispirillum, Olsenella, and Streptococcus, but facilitated the growth of beneficial bacteria negatively correlated with obesity, like Roseburia, Coprococcus, and Bacteroides, along with increasing the short-chain fatty acid levels. It is deduced that the underlying alleviating mechanism of LP was to modulate the hepatic AMPK signaling pathway and gut microbiota by the microbiome−fat−liver axis to alleviate obesity development. In conclusion, as a diet supplement, LP has promising potential in obesity prevention and treatment.

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Systematic evaluation of genome-wide metabolic landscapes in lactic acid bacteria reveals diet- and strain-specific probiotic idiosyncrasies

Cited by 14 publications

References 170 publications

Development of non-alcoholic steatohepatitis is associated with gut microbiota but not with oxysterol enzymes CH25H, EBI2, or CYP7B1 in mice

Development of non-alcoholic steatohepatitis is associated with gut microbiota but not with oxysterol enzymes CH25H, EBI2, or CYP7B1 in mice

Genome-scale metabolic modeling and in silico analysis of opportunistic skin pathogen Cutibacterium acnes

Modulation of the Microbiome–Fat–Liver Axis by Lactic Acid Bacteria: A Potential Alleviated Role in High-Fat-Diet-Induced Obese Mice

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