Recognition and Degradation of Plant Cell Wall Polysaccharides by Two Human Gut Symbionts

Martens, Eric C.; Lowe, Elisabeth C.; Chiang, Herbert C.; Pudlo, Nicholas A.; Wu, Mengmeng; McNulty, Nathan P.; Abbott, D. Wade; Henrissat, Bernard; Gilbert, Harry J.; Bolam, David N.; Gordon, Jeffrey I.

doi:10.1371/journal.pbio.1001221

Cited by 705 publications

(875 citation statements)

References 36 publications

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“…In addition, three pectin lyases and two families of cellulose esterases were detected and these most likely act on plant cell wall polysaccharides. However, consistent with observations that T49 T frequently lacks operon-based genome organisation, we were unable to identify polysaccharide utilisation loci previously reported (Martens et al, 2011) as essential for the degradation of plant pectins. The presence of endoglucanase-acting mannanases, xylanases and pectin lyases may reflect an adaption to the elevated mannan and hemicellulose contents of New Zealand native plants and exotic pines, which are abundant in the geothermal locations from which other Chthonomonas strains were isolated (Stott et al, 2008).…”

Section: Carbohydrate-active Enzymessupporting

confidence: 64%

Genomic analysis of Chthonomonas calidirosea, the first sequenced isolate of the phylum Armatimonadetes

et al. 2014

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Most of the lineages of bacteria have remained unknown beyond environmental surveys using molecular markers. Until the recent characterisation of several strains, the phylum Armatimonadetes (formerly known as 'candidate division OP10') was a dominant and globally-distributed lineage within this 'uncultured majority'. Here we report the first Armatimonadetes genome from the thermophile Chthonomonas calidirosea T49 T and its role as a saccharide scavenger in a geothermal steam-affected soil environment. Phylogenomic analysis indicates T49 T to be related closely to the phylum Chloroflexi. The predicted genes encoding for carbohydrate transporters (27 carbohydrate ATP-binding cassette transporter-related genes) and carbohydrate-metabolising enzymes (including at least 55 putative enzymes with glycosyl hydrolase domains) within the 3.43 Mb genome help explain its ability to utilise a wide range of carbohydrates as well as its inability to break down extracellular cellulose. The presence of only a single class of branched amino acid transporter appears to be the causative step for the requirement of isoleucine for growth. The genome lacks many commonly conserved operons (for example, lac and trp). Potential causes for this, such as dispersion of functionally related genes via horizontal gene transfer from distant taxa or recent genome recombination, were rejected. Evidence suggests T49 T relies on the relatively abundant r-factors, instead of operonic organisation, as the primary means of transcriptional regulation. Examination of the genome with physiological data and environmental dynamics (including interspecific interactions) reveals ecological factors behind the apparent elusiveness of T49 T to cultivation and, by extension, the remaining 'uncultured majority' that have so far evaded conventional microbiological techniques.

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Section: Carbohydrate-active Enzymessupporting

confidence: 64%

Genomic analysis of Chthonomonas calidirosea, the first sequenced isolate of the phylum Armatimonadetes

et al. 2014

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“…These included strong positive association between glucose level and Ruminococcus abundance (glucose is released by ruminococci during fermentation), negative relationship between glucose and Coprococcus (some coprococci use glucose under anaerobic conditions), and positive associations of Acidaminobacter, Coprococcus and Prevotella with acetate, valerate and fumarate, respectively, likely explained by the observed production of these metabolites by the members of these genera (Holdeman and Moore, 1974, Bergey and Holt, 1994, Takahashi and Yamada, 2000, Duncan et al, 2002, Iakiviak et al, 2011. Abundances of genera Bacteroides and Bifidobacterium, which contain many members with large repertoires of carbohydrate-degrading enzymes, were not associated significantly with any of the measured fermentation-derived metabolites, likely due to the ability of these organisms to switch from one carbohydrate to another based on luminal availability and thus produce a variety of fermentation products (Martens et al, 2011). The revealed associations of other genera with specific metabolites shown in Figure 2c have not yet been reported and represent putative novel interactions.…”

Section: Putative Associations Between Intestinal Metabolites and Micmentioning

confidence: 95%

The networks of human gut microbe–metabolite associations are different between health and irritable bowel syndrome

et al. 2015

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The goal of this study was to determine if fecal metabolite and microbiota profiles can serve as biomarkers of human intestinal diseases, and to uncover possible gut microbe-metabolite associations. We employed proton nuclear magnetic resonance to measure fecal metabolites of healthy children and those diagnosed with diarrhea-predominant irritable bowel syndrome (IBS-D). Metabolite levels were associated with fecal microbial abundances. Using several ordination techniques, healthy and irritable bowel syndrome (IBS) samples could be distinguished based on the metabolite profiles of fecal samples, and such partitioning was congruent with the microbiota-based sample separation. Measurements of individual metabolites indicated that the intestinal environment in IBS-D was characterized by increased proteolysis, incomplete anaerobic fermentation and possible change in methane production. By correlating metabolite levels with abundances of microbial genera, a number of statistically significant metabolite-genus associations were detected in stools of healthy children. No such associations were evident for IBS children. This finding complemented the previously observed reduction in the number of microbe-microbe associations in the distal gut of the same cohort of IBS-D children.

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“…[Note that members of the gut microbiota, including Bacteroides spp. represented in the artificial community, are known to impact the mucus layer and mucosal glycans through a variety of means (17)(18)(19).] Although we cannot completely rule out the possibility that ϕHSC03 and ϕHSC04 were first detected at later time points because there had been a selection for mutants that could replicate better, this seems unlikely; their late appearance was a common feature in mice receiving the live p-VLP preparation, and, as noted above, there was no obvious variation in their viral genomes between animals and within a given mouse over time (Fig.…”

Section: Nonsimultaneous Detection Of Viruses and Community Rearrangementioning

confidence: 99%

Gnotobiotic mouse model of phage–bacterial host dynamics in the human gut

Reyes

McNulty

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Bacterial viruses (phages) are the most abundant biological group on Earth and are more genetically diverse than their bacterial prey/ hosts. To characterize their role as agents shaping gut microbial community structure, adult germ-free mice were colonized with a consortium of 15 sequenced human bacterial symbionts, 13 of which harbored one or more predicted prophages. One member, Bacteroides cellulosilyticus WH2, was represented by a library of isogenic transposon mutants that covered 90% of its genes. Once assembled, the community was subjected to a staged phage attack with a pool of live or heat-killed virus-like particles (VLPs) purified from the fecal microbiota of five healthy humans. Shotgun sequencing of DNA from the input pooled VLP preparation plus shotgun sequencing of gut microbiota samples and purified fecal VLPs from the gnotobiotic mice revealed a reproducible nonsimultaneous pattern of attack extending over a 25-d period that involved five phages, none described previously. This system allowed us to (i) correlate increases in specific phages present in the pooled VLPs with reductions in the representation of particular bacterial taxa, (ii) provide evidence that phage resistance occurred because of ecological or epigenetic factors, (iii) track the origin of each of the five phages among the five human donors plus the extent of their genome variation between and within recipient mice, and (iv) establish the dramatic in vivo fitness advantage that a locus within a B. cellulosilyticus prophage confers upon its host. Together, these results provide a defined community-wide view of phage-bacterial host dynamics in the gut.T he human gut is home to tens of trillions of microbial cells representing all three domains of life, although most are bacteria. These organisms collaborate and compete for functional niches and physical locations (habitats). Together, they form a continuously functioning microbial metabolic "organ." The microbial diversity, interpersonal variation, and dynamism of the human gut microbiota make the task of identifying the factors that define community configurations extremely challenging.In some ecosystems, phages maintain high bacterial strain level diversity through lysis of their host strains (constant diversity dynamics model; refs 1, 2). The resulting emptied niche is filled with either an evolved resistant bacterial strain or a taxonomically closely related bacterial species. These dynamics have been observed in open marine environments (1). In contrast, a recent study of 37 healthy adults indicated that a person's fecal microbiota was remarkably stable, with 60% of bacterial strains retained over the course of 5 y (3). Stability followed a power law dynamic that when extrapolated suggests that most strains in an individual's gut community are retained for decades (3). In a metagenomic analysis of virus-like particles (VLPs) purified from the fecal microbiota of healthy adult monozygotic twins and their mothers, sampled over the course of a year, viral community structure exh...

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Recognition and Degradation of Plant Cell Wall Polysaccharides by Two Human Gut Symbionts

Abstract: Competition for nutrients contained in diverse types of plant cell wall-associated polysaccharides may explain the evolution of substrate-specific catabolic gene modules in common bacterial members of the human gut microbiota.

Cited by 705 publications

References 36 publications

Genomic analysis of Chthonomonas calidirosea, the first sequenced isolate of the phylum Armatimonadetes

Genomic analysis of Chthonomonas calidirosea, the first sequenced isolate of the phylum Armatimonadetes

The networks of human gut microbe–metabolite associations are different between health and irritable bowel syndrome

Gnotobiotic mouse model of phage–bacterial host dynamics in the human gut

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