Polysaccharide utilization locus and CAZYme genome repertoires reveal diverse ecological adaptation of Prevotella species

Accetto, Tomaž; Avguštin, Gorazd

doi:10.1016/j.syapm.2015.07.007

Cited by 62 publications

(57 citation statements)

References 56 publications

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“…While most human associated Prevotella spp., particularly those isolated from the oral cavity (e.g., P. intermedia and P. nigrescens ), are specialized on the degradation of nitrogenous compounds (Takahashi and Yamada, ), P. copri is adapted to its environmental niche, where complex polysaccharides are frequently available substrates (Flint et al, ; Accetto and Avguštin, ). Being strictly dependent on a sugar source, P. copri possesses a tremendous number of genes encoding enzymes for the use of a wide range of dietary polysaccharides, such as starch, xylans and pectin (Accetto and Avguštin, ; Kovatcheva‐Datchary et al, ). These polymers are finally degraded into monosaccharides and can enter the central carbon metabolism.…”

Section: Discussionmentioning

confidence: 99%

“…(Flint et al, 2008;Accetto and Avguštin, 2015). Being strictly dependent on a sugar source, P. copri possesses a tremendous number of genes encoding enzymes for the use of a wide range of dietary polysaccharides, such as starch, xylans and pectin (Accetto and Avguštin, 2015;Kovatcheva-Datchary et al, 2015). These polymers are finally degraded into monosaccharides and can enter the central carbon metabolism.…”

Section: Discussionmentioning

confidence: 99%

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Physiology and central carbon metabolism of the gut bacterium Prevotella copri

Franke

Deppenmeier

2018

Molecular Microbiology

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The human gut microbiota is a crucial factor for the host's physiology with respect to health and disease. Metagenomic shotgun sequencing of microbial gut communities revealed that Prevotella copri is one of the most important players in the gastrointestinal tract of many individuals. Because of the importance of this bacterium we analyzed the growth behavior and the central metabolic pathways of P. copri. Bioinformatic data, transcriptome profiling and enzyme activity measurements indicated that the major pathways are based on glycolysis and succinate production from fumarate. In addition, pyruvate can be degraded to acetate and formate. Electron transport phosphorylation depends on fumarate respiration with NADH and reduced ferredoxin as electron donors. In contrast to Bacteroides vulgatus, P. copri showed a more pronounced dependency on the addition of CO or bicarbonate for biomass formation, which is a remarkable difference between P. copri and Bacteroides spp. with important implication in the context of gut microbial competition. The analysis of substrate consumption and product concentrations from many P. copri cultures with different optical densities allowed a prediction of the carbon and electron flow in the central metabolism and a detailed calculation of growth yields as well as carbon and redox balances.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Physiology and central carbon metabolism of the gut bacterium Prevotella copri

Franke

Deppenmeier

2018

Molecular Microbiology

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“…Rumen Prevotella spp. are often referred to as amylolytic and proteolytic, but they also have carbohydrate metabolic capacity (Gardener et al, 1995; Krause et al, 2003; Accetto and Avguštin, 2015; Kishi et al, 2015). Interestingly, the number of COG carbohydrate families classifying as cellulases was on average only 3.2% of the total normalized reads within those sequences classified as COG families involved in carbohydrate metabolism.…”

Section: Discussionmentioning

confidence: 99%

Temporal Metagenomic and Metabolomic Characterization of Fresh Perennial Ryegrass Degradation by Rumen Bacteria

et al. 2016

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Understanding the relationship between ingested plant material and the attached microbiome is essential for developing methodologies to improve ruminant nutrient use efficiency. We have previously shown that perennial ryegrass (PRG) rumen bacterial colonization events follow a primary (up to 4 h) and secondary (after 4 h) pattern based on the differences in diversity of the attached bacteria. In this study, we investigated temporal niche specialization of primary and secondary populations of attached rumen microbiota using metagenomic shotgun sequencing as well as monitoring changes in the plant chemistry using mid-infrared spectroscopy (FT-IR). Metagenomic Rapid Annotation using Subsystem Technology (MG-RAST) taxonomical analysis of shotgun metagenomic sequences showed that the genera Butyrivibrio, Clostridium, Eubacterium, Prevotella, and Selenomonas dominated the attached microbiome irrespective of time. MG-RAST also showed that Acidaminococcus, Bacillus, Butyrivibrio, and Prevotella rDNA increased in read abundance during secondary colonization, whilst Blautia decreased in read abundance. MG-RAST Clusters of Orthologous Groups (COG) functional analysis also showed that the primary function of the attached microbiome was categorized broadly within “metabolism;” predominantly amino acid, carbohydrate, and lipid metabolism and transport. Most sequence read abundances (51.6, 43.8, and 50.0% of COG families pertaining to amino acid, carbohydrate and lipid metabolism, respectively) within these categories were higher in abundance during secondary colonization. Kyoto encyclopedia of genes and genomes (KEGG) pathways analysis confirmed that the PRG-attached microbiota present at 1 and 4 h of rumen incubation possess a similar functional capacity, with only a few pathways being uniquely found in only one incubation time point only. FT-IR data for the plant residues also showed that the main changes in plant chemistry between primary and secondary colonization was due to increased carbohydrate, amino acid, and lipid metabolism. This study confirmed primary and secondary colonization events and supported the hypothesis that functional changes occurred as a consequence of taxonomical changes. Sequences within the carbohydrate metabolism COG families contained only 3.2% of cellulose activities, on average across both incubation times (1 and 4 h), suggesting that degradation of the plant cell walls may be a key rate-limiting factor in ensuring the bioavailability of intra-plant nutrients in a timely manner to the microbes and ultimately the animal. This suggests that a future focus for improving ruminant nutrient use efficiency should be altering the recalcitrant plant cell wall components and/or improving the cellulolytic capacity of the rumen microbiota.

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“…So far, the greatest number of glycan degrading enzymes has been attributed to B. cellulosilyticus , totaling an astonishing 510 CAZYmes [18]. Among Prevotella species, 34 to 107 CAZYmes have been identified per genome [20]. The ability of these bacteria to take on a kaleidoscope of glycans makes them ideally suited to an omnivorous host with a variable diet.…”

Section: The Phylum Bacteroidetesmentioning

confidence: 99%

Microbiome and metabolic disease: revisiting the bacterial phylum Bacteroidetes

et al. 2016

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Bacterial species composition in the gut has emerged as an important factor in obesity and its related metabolic diseases such as type 2 diabetes. Out of thousands of bacterial species-level phylotypes inhabiting the human gut, the majority belong to two dominant phyla, the Bacteroidetes and Firmicutes. Members of the Bacteroidetes in particular have been associated with human metabolic diseases. However, their associations with disease are not always consistent between studies. Delving deeper into the diversity within the Bacteroidetes reveals a vast diversity in genomes and capacities, which partly explain how not all members respond equally to similar environmental conditions in their hosts. Here, we discuss the Bacteroidetes phylum, associations of its members with metabolic phenotypes, and efforts to characterize functionally their interactions with their hosts. Harnessing the Bacteroidetes to promote metabolic health will require a nuanced understanding of how specific strains interact with their microbial neighbors and their hosts under various conditions.

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Polysaccharide utilization locus and CAZYme genome repertoires reveal diverse ecological adaptation of Prevotella species

Cited by 62 publications

References 56 publications

Physiology and central carbon metabolism of the gut bacterium Prevotella copri

Physiology and central carbon metabolism of the gut bacterium Prevotella copri

Temporal Metagenomic and Metabolomic Characterization of Fresh Perennial Ryegrass Degradation by Rumen Bacteria

Microbiome and metabolic disease: revisiting the bacterial phylum Bacteroidetes

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