A carbohydrate-active enzyme (CAZy) profile links successful metabolic specialization of Prevotella to its abundance in gut microbiota

Aakko, Juhani; Pietilä, Sami; Toivonen, Raine; Rokka, Anne; Mokkala, Kati; Laitinen, Kirsi; Elo, Laura L.; Hänninen, Arno

doi:10.1038/s41598-020-69241-2

Cited by 36 publications

(21 citation statements)

References 43 publications

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“…It is worth noting that the CAZyme profile is dynamic and appears to be influenced by not only the available carbohydrates but other factors including non-carbohydrate food sources, mode of delivery, and adult lifestyle (Ye et al, 2019). By extension, inter-individual variability in host CAZymes or the loss of some microbial species with specific or unique CAZymes can profoundly alter how the host interacts with diverse carbohydrate sources (Aakko et al, 2020) thereby altering metabolic functionality of the gut microbiota and potentially also affecting host health. Characterizing the CAZyme complement encoded by the microbial genetic diversity present in an individual host (CAZy-typing) can be useful in predicting carbohydrate pools that the host can metabolize, or which CAZyme families are underrepresented requiring supplementation via microbiota transplantation or probiotics.…”

Section: Introductionmentioning

confidence: 99%

Oral and Gut Microbial Carbohydrate-Active Enzymes Landscape in Health and Disease

et al. 2021

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Inter-individual variability in the microbial gene complement encoding for carbohydrate-active enzymes (CAZymes) can profoundly regulate how the host interacts with diverse carbohydrate sources thereby influencing host health. CAZy-typing, characterizing the microbiota-associated CAZyme-coding genes within a host individual, can be a useful tool to predict carbohydrate pools that the host can metabolize, or identify which CAZyme families are underrepresented requiring supplementation via microbiota transplantation or probiotics. CAZy-typing, moreover, provides a novel framework to search for disease biomarkers. As a proof of concept, we used publicly available metagenomes (935) representing 310 type strain bacterial genomes to establish the link between disease status and CAZymes in the oral and gut microbial ecosystem. The abundance and distribution of 220 recovered CAZyme families in saliva and stool samples from patients with colorectal cancer, rheumatoid arthritis, and type 1 diabetes were compared with healthy subjects. Based on the multivariate discriminant analysis, the disease phenotype did not alter the CAZyme profile suggesting a functional conservation in carbohydrate metabolism in a disease state. When disease and healthy CAZyme profiles were contrasted in differential analysis, CAZyme markers that were underrepresented in type 1 diabetes (15), colorectal cancer (12), and rheumatoid arthritis (5) were identified. Of interest, are the glycosyltransferase which can catalyze the synthesis of glycoconjugates including lipopolysaccharides with the potential to trigger inflammation, a common feature in many diseases. Our analysis has also confirmed the expansive carbohydrate metabolism in the gut as evidenced by the overrepresentation of CAZyme families in the gut compared to the oral site. Nevertheless, each site exhibited specific CAZyme markers. Taken together, our analysis provides an insight into the CAZyme landscape in health and disease and has demonstrated the diversity in carbohydrate metabolism in host-microbiota which can be a sound basis for optimizing the selection of pre, pro, and syn-biotic candidate products.

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Section: Introductionmentioning

confidence: 99%

Oral and Gut Microbial Carbohydrate-Active Enzymes Landscape in Health and Disease

et al. 2021

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“…Referred to as CAZy-typing, the analysis of the repertoires of gut microbiome CAZyme-encoding genes can be used as an indicator to predict the metabolisation of prebiotics on an individual scale [ 159 ]. Indeed, the inconsistent responsiveness of individuals in dietary interventions can be explained by the absence of functional “guilds” able to access and utilise a carbon source [ 160 ].…”

Section: From Fundamental Research To Therapeutic Usementioning

confidence: 99%

Prebiotics and the Human Gut Microbiota: From Breakdown Mechanisms to the Impact on Metabolic Health

et al. 2022

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The colon harbours a dynamic and complex community of microorganisms, collectively known as the gut microbiota, which constitutes the densest microbial ecosystem in the human body. These commensal gut microbes play a key role in human health and diseases, revealing the strong potential of fine-tuning the gut microbiota to confer health benefits. In this context, dietary strategies targeting gut microbes to modulate the composition and metabolic function of microbial communities are of increasing interest. One such dietary strategy is the use of prebiotics, which are defined as substrates that are selectively utilised by host microorganisms to confer a health benefit. A better understanding of the metabolic pathways involved in the breakdown of prebiotics is essential to improve these nutritional strategies. In this review, we will present the concept of prebiotics, and focus on the main sources and nature of these components, which are mainly non-digestible polysaccharides. We will review the breakdown mechanisms of complex carbohydrates by the intestinal microbiota and present short-chain fatty acids (SCFAs) as key molecules mediating the dialogue between the intestinal microbiota and the host. Finally, we will review human studies exploring the potential of prebiotics in metabolic diseases, revealing the personalised responses to prebiotic ingestion. In conclusion, we hope that this review will be of interest to identify mechanistic factors for the optimization of prebiotic-based strategies.

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“…The changes in the abundance of Prevotella were significantly negatively correlated with nitrite content and significantly positively correlated with methylimidazole acetic acid and N-acetyl histamine levels. Prevotella has proteolytic activity, a function similar to that of exopeptidases, with positive effects on protein degradation and utilization of hydrolysis products (Griswold and Mackie, 1997), and plays an important role in carbohydrate utilization (Durb' An et al, 2013;Aakko et al, 2020), indicating that the decrease in Prevotella abundance caused by high-dose β-conglycinin had a more serious negative effect on the response to nitrogenous nutrients and "carbohydrate utilization and metabolism" in hybrid groupers. The decrease in the abundance of Anaerovibrio was significantly negatively correlated with nitrite content and significantly positively correlated with methylimidazole acetic acid, N-acetyl histamine, urocanic acid, creatinine, glutathione, and S-adenosylhomocysteine levels.…”

Section: Correlation Between Distal Intestinal Microbiota and Water Pollutants And Host Healthmentioning

confidence: 99%

Dynamic Alterations of the Distal Intestinal Microbiota, Transcriptome, and Metabolome of Hybrid Grouper by β -Conglycinin With Reconciliations by Sodium Butyrate in Feed

et al. 2021

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Different doses of β-conglycinin produce different regulations on the intestinal health of aquatic animals, affecting the absorption of nutrients, indirectly changing water quality. Sodium butyrate (NaB) can effectively alleviate the negative effects caused by high-dose β-conglycinin. We investigated the positive response to low-dose (1.5%, bL) and negative response to high-dose (6.0%, bH) β-conglycinin and supplementation with NaB (6.0% β-conglycinin + 0.13% NaB, bHNaB) in terms of water pollutants, microbiota, transcriptome, and metabolome in hybrid grouper (Epinephelus fuscoguttatus♀ × E. lanceolatus♂). The ammonia nitrogen, nitrite, total nitrogen, and total phosphorus contents were significantly higher in the water from bH than from FMb, bL, and bHNaB. Supplementing with NaB significantly reduced the ammonia nitrogen, nitrite, total nitrogen, and total phosphorus contents. Low-dose β-conglycinin increased the relative abundance of Pelagibacterium, Pediococcus, Staphylococcus, and Lactobacillus and promoted the “ribosome,” “peroxisome proliferator-activated receptor (PPAR) signaling” and “histidine metabolism.” High-dose β-conglycinin increased the relative abundance of pathogenic bacteria Ralstonia and Photobacterium and inhibited the “cell cycle” “PPAR signaling” and “starch and proline metabolism.” NaB supplementation at high-dose β-conglycinin reduced the Ralstonia and Photobacterium abundance and promoted the “cell cycle,” “linoleic acid metabolism,” and “ABC transporters.” Overall, these results reveal differences in the effects of high- and low-dose β-conglycinin, as well as NaB supplementation, on the utilization of proteins, carbohydrates, and lipids and on substance transport and signaling among distal intestinal cells of hybrid grouper. A total of 15 differential metabolite biomarkers were identified: FMb vs. bL contained 10-methylimidazole acetic acid, N-acetyl histamine, urocanic acid, creatinine, glutathione, taurine, nervonic acid, stearic acid, docosanoic acid, and D-serine; FMb vs. bH contained 4-L-fucose, sucrose, α,α-trehalose, and quercetin; and bH vs. bHNaB contained 4-N-acetyl histamine, urocanic acid, creatinine, and S-adenosylhomocysteine, respectively. Our study provides new insights into the regulation of intestinal health by β-conglycinin in aquatic animals and the protective mechanism of NaB.

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A carbohydrate-active enzyme (CAZy) profile links successful metabolic specialization of Prevotella to its abundance in gut microbiota

Cited by 36 publications

References 43 publications

Oral and Gut Microbial Carbohydrate-Active Enzymes Landscape in Health and Disease

Oral and Gut Microbial Carbohydrate-Active Enzymes Landscape in Health and Disease

Prebiotics and the Human Gut Microbiota: From Breakdown Mechanisms to the Impact on Metabolic Health

Dynamic Alterations of the Distal Intestinal Microbiota, Transcriptome, and Metabolome of Hybrid Grouper by β -Conglycinin With Reconciliations by Sodium Butyrate in Feed

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