Biomass utilization by gut microbiomes White, Bryan A; Lamed, Raphael; Bayer, Edward A ...
Annual review of microbiology,
01/2014, Letnik:
68
Journal Article
Recenzirano
Mammals rely entirely on symbiotic microorganisms within their digestive tract to gain energy from plant biomass that is resistant to mammalian digestive enzymes. Especially in herbivorous animals, ...specialized organs (the rumen, cecum, and colon) have evolved that allow highly efficient fermentation of ingested plant biomass by complex anaerobic microbial communities. We consider here the two most intensively studied, representative gut microbial communities involved in degradation of plant fiber: those of the rumen and the human large intestine. These communities are dominated by bacteria belonging to the Firmicutes and Bacteroidetes phyla. In Firmicutes, degradative capacity is largely restricted to the cell surface and involves elaborate cellulosome complexes in specialized cellulolytic species. By contrast, in the Bacteroidetes, utilization of soluble polysaccharides, encoded by gene clusters (PULs), entails outer membrane binding proteins, and degradation is largely periplasmic or intracellular. Biomass degradation involves complex interplay between these distinct groups of bacteria as well as (in the rumen) eukaryotic microorganisms.
Highlights • Metagenomics has revolutionised research into human intestinal microbes. • Limitations of metagenomics mean that culturing and phylogeny remain relevant. • Phylogeny and culture will be ...crucial for the development of new microbial therapeutics. • A combination of culturing and metagenomics is needed to gain new insights into functionality.
A decrease in the abundance and biodiversity of intestinal bacteria within the Firmicutes phylum has been associated with inflammatory bowel disease (IBD). In particular, the anti-inflammatory ...bacterium Faecalibacterium prausnitzii, member of the Firmicutes phylum and one of the most abundant species in healthy human colon, is underrepresented in the microbiota of IBD patients. The aim of this study was to investigate the immunomodulatory properties of F. prausnitzii strain A2-165, the biofilm forming strain HTF-F and the extracellular polymeric matrix (EPM) isolated from strain HTF-F. For this purpose, the immunomodulatory properties of the F. prausnitzii strains and the EPM were studied in vitro using human monocyte-derived dendritic cells. Then, the capacity of the F. prausnitzii strains and the EPM of HTF-F to suppress inflammation was assessed in vivo in the mouse dextran sodium sulphate (DSS) colitis model. The F. prausnitzii strains and the EPM had anti-inflammatory effects on the clinical parameters measured in the DSS model but with different efficacy. The immunomodulatory effects of the EPM were mediated through the TLR2-dependent modulation of IL-12 and IL-10 cytokine production in antigen presenting cells, suggesting that it contributes to the anti-inflammatory potency of F. prausnitzii HTF-F. The results show that F. prausnitzii HTF-F and its EPM may have a therapeutic use in IBD.
A novel lanC-like sequence was identified from the dominant human gut bacterium Blautia obeum strain A2-162. This sequence was extended to reveal a putative lantibiotic operon with biosynthetic and ...transport genes, two sets of regulatory genes, immunity genes, three identical copies of a nisin-like lanA gene with an unusual leader peptide, and a fourth putative lanA gene. Comparison with other nisin clusters showed that the closest relationship was to nisin U. B. obeum A2-162 demonstrated antimicrobial activity against Clostridium perfringens when grown on solid medium in the presence of trypsin. Fusions of predicted nsoA structural sequences with the nisin A leader were expressed in Lactococcus lactis containing the nisin A operon without nisA. Expression of the nisA leader sequence fused to the predicted structural nsoA1 produced a growth defect in L. lactis that was dependent upon the presence of biosynthetic genes, but failed to produce antimicrobial activity. Insertion of the nso cluster into L. lactis MG1614 gave an increased immunity to nisin A, but this was not replicated by the expression of nsoI. Nisin A induction of L. lactis containing the nso cluster and nisRK genes allowed detection of the NsoA1 pre-peptide by Western hybridization. When this heterologous producer was grown with nisin induction on solid medium, antimicrobial activity was demonstrated in the presence of trypsin against C. perfringens, Clostridium difficile and L. lactis. This research adds to evidence that lantibiotic production may be an important trait of gut bacteria and could lead to the development of novel treatments for intestinal diseases.
Scope
Plant secondary metabolites, such as phenolic acids are commonly associated with benefits for human health. Two of the most abundant phenylpropanoid‐derived compounds detected in human faecal ...samples are phenylacetic acid (PAA) and 4‐hydroxylphenylacetic acid (4‐hydroxyPAA). Although they have the potential to be derived from diets rich in plant‐based foods, evidence suggests that these compounds can be derived from the microbial fermentation of aromatic amino acids (AAAs) in the colon.
Methods and results
To identify the bacteria responsible, 26 strains representing 25 of the dominant human colonic species were screened for phenyl metabolite formation. Seven strains produced significant amounts of both PAA and 4‐hydroxyPAA. These included five out of seven Bacteroidetes (Bacteroides thetaiotaomicron, Bacteroides eggerthii, Bacteroides ovatus, Bacteroides fragilis, Parabacteroides distasonis), and two out of 17 Firmicutes (Eubacterium hallii and Clostridium bartlettii). These species also produced indole‐3‐acetic acid (IAA), the corresponding tryptophan metabolite, but C. bartlettii showed 100 times higher IAA production than the other six strains. Four strains were further tested and PAA formation was substantially increased by phenylalanine, 4‐hydroxyPAA by tyrosine and IAA by tryptophan.
Conclusion
This study demonstrates that certain microbial species have the ability to ferment all three AAAs and that protein fermentation is the likely source of major phenylpropanoid‐derived metabolites in the colon.
We describe a new degenerate real-time PCR approach to simultaneously quantify phylogenetically different butyrate-producing bacteria based on the detection of butyryl-coenzyme A (CoA) CoA ...transferase genes. This pathway is present in numerically important groups of butyrate producers within the human colon, and thus this assay estimates the butyrate-producing ability of the microbiota.
Summary
Interspecies cross‐feeding is a fundamental factor in anaerobic microbial communities. In the human colon, formate is produced by many bacterial species but is normally detected only at low ...concentrations. Ruminococcus bromii produces formate, ethanol and acetate in approximately equal molar proportions in pure culture on RUM‐RS medium with 0.2% Novelose resistant starch (RS3) as energy source. Batch co‐culturing on starch with the acetogen Blautia hydrogenotrophica however led to the disappearance of formate and increased levels of acetate, which is proposed to occur through the routing of formate via the Wood Ljungdahl pathway of B. hydrogenotrophica. We investigated these inter‐species interactions further using RNAseq to examine gene expression in continuous co‐cultures of R. bromii and B. hydrogenotrophica. Transcriptome analysis revealed upregulation of B. hydrogenotrophica genes involved in the Wood‐Ljungdahl pathway and of a 10 gene cluster responsible for increased branched chain amino acid fermentation in the co‐cultures. Cross‐feeding between formate‐producing species and acetogens may be a significant factor in short chain fatty acid formation in the colon contributing to high rates of acetate production. Transcriptome analysis also indicated competition for the vitamin thiamine and downregulation of dissimilatory sulfate reduction and key redox proteins in R. bromii in the co‐cultures, thus demonstrating the wide‐ranging consequences of inter‐species interactions in this model system.
Cross-feeding is an important metabolic interaction mechanism of bacterial groups inhabiting the human colon and includes features such as the utilization of acetate by butyrate-producing bacteria as ...may occur between Bifidobacterium and Faecalibacterium genera. In this study, we assessed the utilization of different carbon sources (glucose, starch, inulin and fructooligosaccharides) by strains of both genera and selected the best suited combinations for evidencing this cross-feeding phenomenon. Co-cultures of Bifidobacterium adolescentis L2–32 with Faecalibacterium prausnitzii S3/L3 with fructooligosaccharides as carbon source, as well as with F. prausnitzii A2–165 in starch, were carried out and the production of short-chain fatty acids was determined. In both co-cultures, acetate levels decreased between 8 and 24 h of incubation and were lower than in the corresponding B. adolescentis monocultures. In contrast, butyrate concentrations were higher in co-cultures as compared to the respective F. prausnitzii monocultures, indicating enhanced formation of butyrate by F. prausnitzii in the presence of the bifidobacteria. Variations in the levels of acetate and butyrate were more pronounced in the co-culture with fructooligosaccharides than with starch. Our results provide a clear demonstration of cross-feeding between B. adolescentis and F. prausnitzii.
The article provides the first experimental demonstration of enhanced butyrate formation by a cross feeding mechanisms betweeen Faecalibacterium prausnitzii, a comensal bacteria of the human colon, with Bifidobacterium adolescentis, one of the most abundant bifidobacteria from the adult's intestinal microbiota.
Degradation of lignocellulosic plant material in the mammalian digestive tract is accomplished by communities of anaerobic microorganisms that exist in symbiotic association with the host. Catalytic ...domains and substrate‐binding modules concerned with plant polysaccharide degradation are found in a variety of anaerobic bacteria, fungi, and protozoa from the mammalian gut. The organization of plant cell wall–degrading enzymes, however, varies widely. The cellulolytic gram‐positive bacterium Ruminococcus flavefaciens produces an elaborate cellulosomal enzyme complex that is anchored to the bacterial cell wall; assembly of the complex involves at least five different dockerin:cohesin specificities, and the R. flavefaciens genome encodes at least 180 dockerin‐containing proteins that encompass a wide array of catalytic and binding activities. On the other hand, in the cellulolytic protozoan, Polyplastron multivesiculatum, individual plant cell wall–degrading enzymes appear to be secreted into food vacuoles, while the gram‐negative bacterium Prevotella bryantii appears to possess a sequestration‐type system for the utilization of soluble xylans. The system that is employed for polysaccharide utilization must play a major role in defining the ecological niche that each organism occupies within a complex gut community. 16S rRNA analyses are also revealing uncultured bacterial species closely adherent to fibrous substrates in the rumen and in the large intestine of animals and humans. The true complexity, both at a single organism and community level, of the microbial enzyme systems that allow animals to digest plant material is beginning to become apparent.
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