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B. plebeius contains two endo-acting porphyranases, BpGH16B and BpGH86A, and an agarase, BpGH16A. ( A ) Activity test on agar plate revealed similar agarase activity of BpGH16A to the previously characterized ZgAgaA from Z. galactanivorans (positive control). BpGH16B and GH86A were inactive on this substrate. Heat-inacti- vated enzymes served as control. (Scale bar: 1 cm.) ( B ) Relative activity of BpGH16B and BpGH86A with porphyran as substrate measured by reducing sugar assays showed porphyranolytic activity. ( C ) The reaction products of BpGH16B and BpGH86A, incubated with native porphyran, were analyzed by fl uorophore-assisted PACE showing a ladder-like pattern typical for endo-acting glycoside hydrolases. ( D ) Comparative hydrolysis of native and pure porphyran by B. plebeius enzymes and ZgAgaA showing that BpGH16B and BpGH86A have higher activity than the agarases. ( E ) TLC analysis of degradation products reveals that BpGH16B releases similar reaction products to the previously characterized ZgPorA (positive control), which releases L6S-G ∼ and L6S-G-L6S-G ∼ as major products (14), whereas BpGH86A releases mainly the larger oligosaccharide L6S-G-L6S-G ∼ . Notably, these products are not released by the previously characterized agarase ZgAgaA (negative control). BpGH16A has an agarase-like reaction pattern similar to ZgAgaA. Data in D are mean and SD of independent enzymatic replicates.
Source publication
Humans host an intestinal population of microbes-collectively referred to as the gut microbiome-which encode the carbohydrate active enzymes, or CAZymes, that are absent from the human genome. These CAZymes help to extract energy from recalcitrant polysaccharides. The question then arises as to if and how the microbiome adapts to new carbohydrate s...
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... from marine seaweed-degrading microbes; these homologs have previously demonstrated activity on porphyran. This finding sug- gested that agarose, porphyran, or even carrageenan may be nutrients for this gut microbe. Thus, we used these three galactans as substrates and observed that B. plebeius grew specifically on porphyran (SI Appendix, Fig. S2A). To test whether this result was an isolated case or if these common algal food galactans are ca- tabolized by other human gut microbes, we screened an additional collection of 291 human gut Bacteroidetes (see SI Appendix for details) and identified several carrageenolytic and agarolytic bacteria. One isolate, B. uniformis NP1, grew ...
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... this result was an isolated case or if these common algal food galactans are ca- tabolized by other human gut microbes, we screened an additional collection of 291 human gut Bacteroidetes (see SI Appendix for details) and identified several carrageenolytic and agarolytic bacteria. One isolate, B. uniformis NP1, grew on agarose (SI Ap- pendix, Fig. S2B) and showed reduced growth on porphyran, whereas another, B. thetaiotaomicron VPI-3731, exhibited growth specificity for carrageenan (SI Appendix, Fig. S2C). Together, these growth experiments showed that human gut bacteria catabolize seaweed carbohydrates and that each of these strains is specific for a certain type of red algal ...
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... of 291 human gut Bacteroidetes (see SI Appendix for details) and identified several carrageenolytic and agarolytic bacteria. One isolate, B. uniformis NP1, grew on agarose (SI Ap- pendix, Fig. S2B) and showed reduced growth on porphyran, whereas another, B. thetaiotaomicron VPI-3731, exhibited growth specificity for carrageenan (SI Appendix, Fig. S2C). Together, these growth experiments showed that human gut bacteria catabolize seaweed carbohydrates and that each of these strains is specific for a certain type of red algal galactan. To further understand the molecular mechanism of the degradation of such galactans, we focused on the PUL of B. plebeius for which the whole genome ...
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... BpGH16B, and BpGH86A were assessed for agar- olytic and porphyranolytic activity, whereas BpGH86B could not be expressed. BpGH16A was active on solid agarose, supporting its predicted agarolytic function, whereas BpGH16B and also BpGH86A were inactive on this substrate (Fig. 2A); thus, we also tested their activity on native and pure porphyran (Fig. 2B). Al- though agarases possess comparable activities on native por- phyran, they show significantly lower activity on pure porphyran, which allows one to differentiate between porphyranases and agarases (4). Both BpGH16B and BpGH86A were active on native and pure ...
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... BpGH16B, and BpGH86A were assessed for agar- olytic and porphyranolytic activity, whereas BpGH86B could not be expressed. BpGH16A was active on solid agarose, supporting its predicted agarolytic function, whereas BpGH16B and also BpGH86A were inactive on this substrate (Fig. 2A); thus, we also tested their activity on native and pure porphyran (Fig. 2B). Al- though agarases possess comparable activities on native por- phyran, they show significantly lower activity on pure porphyran, which allows one to differentiate between porphyranases and agarases (4). Both BpGH16B and BpGH86A were active on native and pure porphyran preparations (Fig. 2B), whereas BpGH16A showed a significantly ...
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... tested their activity on native and pure porphyran (Fig. 2B). Al- though agarases possess comparable activities on native por- phyran, they show significantly lower activity on pure porphyran, which allows one to differentiate between porphyranases and agarases (4). Both BpGH16B and BpGH86A were active on native and pure porphyran preparations (Fig. 2B), whereas BpGH16A showed a significantly lower level of activity on pure and native porphyran preparations (Fig. 2D), comparable to the β-agarase ZgAgaA from Zobellia galactanivorans (22). showing that BpGH16B and BpGH86A have higher activity than the agarases. (E) TLC analysis of deg- radation products reveals that BpGH16B releases ...
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... native por- phyran, they show significantly lower activity on pure porphyran, which allows one to differentiate between porphyranases and agarases (4). Both BpGH16B and BpGH86A were active on native and pure porphyran preparations (Fig. 2B), whereas BpGH16A showed a significantly lower level of activity on pure and native porphyran preparations (Fig. 2D), comparable to the β-agarase ZgAgaA from Zobellia galactanivorans (22). showing that BpGH16B and BpGH86A have higher activity than the agarases. (E) TLC analysis of deg- radation products reveals that BpGH16B releases similar reaction products to the previously charac- terized ZgPorA (positive control), which releases L6S-G∼ and ...
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... with the fluo- rophore 2-aminoacridone (AMAC) and analyzed by carbohydrate polyacrylamide gel electrophoresis (PACE). Both BpGH86A and BpGH16A successively degraded the high-molecular-weight poly- saccharide into smaller oligosaccharides of random size, apparent in the ladder-type pattern that is typical for endo-acting glycoside hydrolases (Fig. 2C). One well-resolved degradation product from both enzymes corresponded to a band that had the same mobility as an AMAC-labeled tetra-oligosaccharide standard derived from porphyran (L6S-G-L6S-G-AMAC), which is consistent with cleavage of the β-glycosidic linkage (for sugar residue nomencla- ture, see SI Appendix, Fig. S1). We further ...
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... corresponded to a band that had the same mobility as an AMAC-labeled tetra-oligosaccharide standard derived from porphyran (L6S-G-L6S-G-AMAC), which is consistent with cleavage of the β-glycosidic linkage (for sugar residue nomencla- ture, see SI Appendix, Fig. S1). We further used TLC to analyze the reaction products of the different enzymes (Fig. 2E). BpGH16B showed a reaction profile similar to the β-porphyranase ZgPorA from Z. galactanivorans, with L6S-G∼ as a major end product (14). BpGH86A produced predominantly larger oligosaccharides, the smallest of which was the tetra-oligosaccharide L6S-G-L6S-G∼. Consistent with its agarolytic activity, BpGH16A had a different reaction ...
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Citations
... Yet, there are also links between the gut and the environmental microbiomes as previously reported, such as the alginate lyase and carrageenase, which are expected to be present in the marine microbiome (25). However, these two enzymes are also found in the gut microbiome as a result of horizontal gene transfer from marine to gut microbes due to the traditional diet on seaweeds of Japanese (25)(26)(27). ...
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IMPORTANCE
Omics tools are used to explore adaptive mechanism of microbes in diverse systems, but the advantages and limitations of different omics tools remain skeptical. Here, we reported distinct profiles in microbial secretory enzyme composition revealed by different omics methods. In general, the predicted function from metagenomic analysis decoupled from the expression of corresponding transcripts/proteins. Linking omics results to taxonomic origin, functional capability, substrate specificity, secretion preference, and enzymatic activity measurement suggested the substrate's source, concentration and stoichiometry impose strong filtering on the expression of extracellular enzymes, which may overwrite the genetic potentials. Our results present an integrated perspective on the need for multi-dimensional characterization of microbial adaptation in a changing environment.
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... M icroorganisms capable of degrading agar (agarolytic) are important for under standing carbon cycling in marine systems, interactions with agar-producing organisms, and human digestion, and have various biotechnological applications (1)(2)(3)(4)(5)(6)(7). Agar degradation is a widespread phenotype, conferred by multiple different agarases in the CAZyme glycoside hydrolase family with unique agar bond specificities that are deployed in a variety of combinations depending on the organism (3,(8)(9)(10)(11). ...
Here we present the genomes of four marine agarolytic bacteria belonging to the Bacteroidota and Proteobacteria. Two genomes are closed and two are in draft form, but all are at least 99% complete and offer new opportunities to study agar-degradation in marine bacteria.
... Our study indicates that the genome of B. uniformis F18-22 encodes many CAZymes, including glycoside hydrolases (GHs), glycosyltransferases (GTs), polysaccharide lyases (PLs), carbohydrate esterases (CEs), carbohydrate-binding modules (CBMs) and auxiliary activities (AAs). CAZymes are the most important enzymes for the metabolism of complex carbohydrates in the human diet [19][20][21][22]. These results indicate that B. uniformis F18-22 might be able to ferment and utilize a wide range of dietary polysaccharides in the gut. ...
Previous studies have demonstrated that the intestinal abundance of Bacteroides uniformis is significantly higher in healthy controls than that in patients with ulcerative colitis (UC). However, what effect B. uniformis has on the development of UC has not been characterized. Here, we show for the first time that B. uniformis F18-22, an alginate-fermenting bacterium isolated from the healthy human colon, protects against dextran-sulfate-sodium (DSS)-induced UC in mice. Specifically, oral intake of B. uniformis F18-22 alleviated colon contraction, improved intestinal bleeding and attenuated mucosal damage in diseased mice. Additionally, B. uniformis F18-22 improved gut dysbiosis in UC mice by increasing the abundance of anti-inflammatory acetate-producing bacterium Eubacterium siraeum and decreasing the amount of pro-inflammatory pathogenetic bacteria Escherichia-Shigella spp. Moreover, B. uniformis F18-22 was well-tolerated in mice and showed no oral toxicity after repeated daily administration for 28 consecutive days. Taken together, our study illustrates that B. uniformis F18-22 is a safe and novel probiotic bacterium for the treatment of UC from the healthy human colon.
... Carbohydrate-active enzymes (CAZymes), including glycoside hydrolases (GHs), glycosyltransferases (GTs), polysaccharide lyases (PLs), carbohydrate esterases (CEs), carbohydrate-binding modules (CBMs), and auxiliary activities (AAs), are the most important catalytic enzymes for the metabolism of complex dietary polysaccharides in the human gut [5,[23][24][25][26]. Bacteroides spp. is armed with a plethora of finely tuned CAZymes and has been proposed as a keystone genus for the degradation of complex natural polysaccharides in the human colon [23][24][25][26]. ...
... Carbohydrate-active enzymes (CAZymes), including glycoside hydrolases (GHs), glycosyltransferases (GTs), polysaccharide lyases (PLs), carbohydrate esterases (CEs), carbohydrate-binding modules (CBMs), and auxiliary activities (AAs), are the most important catalytic enzymes for the metabolism of complex dietary polysaccharides in the human gut [5,[23][24][25][26]. Bacteroides spp. is armed with a plethora of finely tuned CAZymes and has been proposed as a keystone genus for the degradation of complex natural polysaccharides in the human colon [23][24][25][26]. For example, Bacteroides xylanisolvens AY11-1, a probiotic anaerobe isolated from the healthy human colon, could degrade and ferment alginate in our daily diet [7]. ...
Dietary intake of the sulfated polysaccharide from edible alga E. clathrata (ECP) has recently been illustrated to attenuate ulcerative colitis (UC) by targeting gut dysbiosis in mice. However, ECP is not easily absorbed in the gut and, as a potential candidate for next-generation prebiotics development, how it is fermented by human gut microbiota has not been characterized. Here, using in vitro anaerobic fermentation and 16S high-throughput sequencing, we illustrate for the first time the detailed fermentation characteristics of ECP by the gut microbiota of nine UC patients. Our results indicated that, compared to that of glucose, fermentation of ECP by human gut microbiota produced a higher amount of anti-inflammatory acetate and a lower amount of pro-inflammatory lactate. Additionally, ECP fermentation helped to shape a more balanced microbiota composition with increased species richness and diversity. Moreover, ECP significantly stimulated the growth of anti-colitis bacteria in the human gut, including Bacteroides thetaiotaomicron, Bacteroides ovatus, Blautia spp., Bacteroides uniformis, and Parabacteroides spp. Altogether, our study provides the first evidence for the prebiotic effect of ECP on human gut microbiota and sheds new light on the development of ECP as a novel prebiotic candidate for the prevention and potential treatment of UC.
... CAZymes display exquisite specificity that distinguishes the carbohydrate moiety and type of glycosidic bond; hence, the CAZyme gene composition within a PUL can provide information on the structure of its targeted polysaccharide [19,21,23]. Bacteroidetes inhabiting different ecological niches with different substrate availability are often equipped with distinct PUL reservoirs [26][27][28] with laterally acquired CAZyme genes playing a potentially important role in their niche expansion [29][30][31]. ...
... A phage integrase, specifically a tyrosine recombinase (gene id: APDGNPDO_02609), is located about 30 genes upstream of the arabinan PUL and could be responsible for the transfer. Similar phage integrases have also been reported around two other laterally acquired PULs and have been suggested as important elements for the integration of external PUL into genomic DNA [29,30]. Finally, through phylogenetic analyses, we validated that the MTRN7 arabinan PUL was likely acquired from coastal/land Bacteroidetes (see supplementary data for detailed results, Fig. S10). ...
Background
Hadal trenches (>6000 m) are the deepest oceanic regions on Earth and depocenters for organic materials. However, how these enigmatic microbial ecosystems are fueled is largely unknown, particularly the proportional importance of complex polysaccharides introduced through deposition from the photic surface waters above. In surface waters, Bacteroidetes are keystone taxa for the cycling of various algal-derived polysaccharides and the flux of carbon through the photic zone. However, their role in the hadal microbial loop is almost unknown.
Results
Here, culture-dependent and culture-independent methods were used to study the potential of Bacteroidetes to catabolize diverse polysaccharides in Mariana Trench waters. Compared to surface waters, the bathypelagic (1000–4000 m) and hadal (6000–10,500 m) waters harbored distinct Bacteroidetes communities, with Mesoflavibacter being enriched at ≥ 4000 m and Bacteroides and Provotella being enriched at 10,400–10,500 m. Moreover, these deep-sea communities possessed distinct gene pools encoding for carbohydrate active enzymes (CAZymes), suggesting different polysaccharide sources are utilised in these two zones. Compared to surface counterparts, deep-sea Bacteroidetes showed significant enrichment of CAZyme genes frequently organized into polysaccharide utilization loci (PULs) targeting algal/plant cell wall polysaccharides (i.e., hemicellulose and pectin), that were previously considered an ecological trait associated with terrestrial Bacteroidetes only. Using a hadal Mesoflavibacter isolate (MTRN7), functional validation of this unique genetic potential was demonstrated. MTRN7 could utilize pectic arabinans, typically associated with land plants and phototrophic algae, as the carbon source under simulated deep-sea conditions. Interestingly, a PUL we demonstrate is likely horizontally acquired from coastal/land Bacteroidetes was activated during growth on arabinan and experimentally shown to encode enzymes that hydrolyze arabinan at depth.
Conclusions
Our study implies that hadal Bacteroidetes exploit polysaccharides poorly utilized by surface populations via an expanded CAZyme gene pool. We propose that sinking cell wall debris produced in the photic zone can serve as an important carbon source for hadal heterotrophs and play a role in shaping their communities and metabolism.
... Members of the phylum Bacteroidetes are selected in such glycan-rich environments (McKee et al., 2021). Recent studies showed the utilization of a diverse range of algal glycans by members of this phylum (e.g., Barbeyron et al., 2016;Beidler et al., 2023;Ficko-Blean et al., 2017;Hehemann et al., 2012;Reisky et al., 2019;Robb et al., 2022;Unfried et al., 2018). Their carbohydrate-active enzymes, or CAZymes, are often co-located with transporters and regulatory proteins in polysaccharide utilization loci (PULs) within bacterial genomes (Martens et al., 2009). ...
Marine Bacteroidetes that degrade polysaccharides contribute to carbon cycling in the ocean. Organic matter, including glycans from terrestrial plants, might enter the oceans through rivers. Whether marine bacteria degrade structurally related glycans from diverse sources including terrestrial plants and marine algae was previously unknown. We show that the marine bacterium Flavimarina sp. Hel_I_48 encodes two polysaccharide utilization loci (PULs) which degrade xylans from terrestrial plants and marine algae. Biochemical experiments revealed activity and specificity of the encoded xylanases and associated enzymes of these PULs. Proteomics indicated that these genomic regions respond to glucuronoxylans and arabinoxylans. Substrate specificities of key enzymes suggest dedicated metabolic pathways for xylan utilization. Some of the xylanases were active on different xylans with the conserved β-1,4-linked xylose main chain. Enzyme activity was consistent with growth curves showing Flavimarina sp. Hel_I_48 uses structurally different xylans. The observed abundance of related xylan-degrading enzyme repertoires in genomes of other marine Bacteroidetes indicates similar activities are common in the ocean. The here presented data show that certain marine bacteria are genetically and biochemically variable enough to access parts of structurally diverse xylans from terrestrial plants as well as from marine algal sources.
... Most studies focused on the effects of gut microbiota as a whole on transforming and degrading the common metabolites in diet, such as catabolizing phenylalanine into indole and phenylacetate [3]. Moreover, the modulation of common bioactive metabolites mainly from plants, pharmaceuticals, and other environmental chemicals in gut intestines have also received immense interest [4,5]. However, what types of specific gut microbial strains and how they function in modulating specific intermediate metabolites in diet still remain largely unclear. ...
Gut microbiota have important implications for health by affecting the metabolism of diet and drugs. However, the specific microbial mediators and their mechanisms in modulating specific key intermediate metabolites from fungal origins still remain largely unclear. Toluquinol, as a key versatile precursor metabolite, is commonly distributed in many fungi, including Penicillium species and their strains for food production. The common 17 gut microbes were cultivated and fed with and without toluquinol. Metabolic analysis revealed that four strains, including the predominant Enterococcus species, could metabolize toluquinol and produce different metabolites. Chemical investigation on large-scale cultures led to isolation of four targeted metabolites and their structures were characterized with NMR, MS, and X-ray diffraction analysis, as four toluquinol derivatives (1–4) through O1/O4-acetyl and C5/C6-methylsulfonyl substitutions, respectively. The four metabolites were first synthesized in living organisms. Further experiments suggested that the rare methylsulfonyl groups in 3–4 were donated from solvent DMSO through Fenton’s reaction. Metabolite 1 displayed the strongest inhibitory effect on cancer cells A549, A2780, and G401 with IC50 values at 0.224, 0.204, and 0.597 μM, respectively, while metabolite 3 displayed no effect. Our results suggest that the dominant Enterococcus species could modulate potential precursors of fungal origin and change their biological activity.
... (Figure 5C). [17][18][19], and, since CAZymes are required for the metabolism of marine algae oligosaccharides [19,20], it is therefore reasonable that different enterotypes of human gut microbiota would have varying effects on the fermentation processes of QOS, KOS, and AOS. Only taxa with an LDA score >2 are listed. ...
... (Figure 5C). [17][18][19], and, since CAZymes are required for the metabolism of marine algae oligosaccharides [19,20], it is therefore reasonable that different enterotypes of human gut microbiota would have varying effects on the fermentation processes of QOS, KOS, and AOS. Only taxa with an LDA score >2 are listed. ...
The human gut microbiota plays a critical role in the metabolism of dietary carbohydrates. Previous studies have illustrated that marine algae oligosaccharides could be utilized and readily fermented by human gut microbiota. However, the human gut microbiota is classified into three different enterotypes, and how this may affect the fermentation processes of marine algae oligosaccharides has not been studied. Here, using in vitro fermentation and 16 S high-throughput sequencing techniques, we demonstrate that the human gut microbiota has an enterotype-specific effect on the fermentation outcomes of marine algae oligosaccharides. Notably, microbiota with a Bacteroides enterotype was more proficient at fermenting carrageenan oligosaccharides (KOS) as compared to that with a Prevotella enterotype and that with an Escherichia enterotype. Interestingly, the prebiotic effects of marine algae oligosaccharides were also found to be enterotype dependent. Altogether, our study demonstrates an enterotype-specific effect of human gut microbiota on the fermentation of marine algae oligosaccharides. However, due to the availability of the fecal samples, only one sample was used to represent each enterotype. Therefore, our research is a proof-of-concept study, and we anticipate that more detailed studies with larger sample sizes could be conducted to further explore the enterotype-specific prebiotic effects of marine oligosaccharides.
... xylanisolvens and B. cellulosilyticus, and B. vulgatus/B. dorei and B. fragilis) (see Fig. 3A for a phylogenetic tree based on conserved housekeeping genes) (31,32). It is interesting to directly compare B. fragilis and B. vulgatus/B. ...
... One hypothesis to explain this observation is that some B. ovatus and B. xylanisolvens strains have gained the ability to utilize O-glycans relative to an ancestor that lacked this phenotype. If so, the PULs they express during O-glycan degradation might be unique to their genomes and may indicate lateral gene transfer (LGT), as has been the case for the acquisition of phenotypes such as porphyran, agarose, and l-carrageenan utilization in gut Bacteroides, which are all components of integrative conjugative elements or mobilizable plasmids (31,40). An alternative hypothesis is that some B. ovatus and B. xylanisolvens strains are in the process of losing this ability from a common ancestor. ...
... Similar to other bacteria, we observed that many accessory genes in the B. ovatus and B. xylanisolvens pangenome are located in contiguous clusters or "islands," often involving PULs or capsular polysaccharide synthesis gene cluster (Table S2a). In contrast to previously identified Bacteroides PULs that have more obviously been subjects of lateral transfer (31,40,41) and are associated with integrative and conjugative elements (ICEs), most of the variable genomic regions that we identified were not associated with functions indicative of mobile DNA. Instead, these regions are often located precisely in between one or more core genes (i.e., those common to all seven strains; herein referred to as "genomic nodes") that flank each side of the variable gene segment ( Fig. 5A and B). ...
Symbiotic bacteria are responsible for the majority of complex carbohydrate digestion in the human colon. Since the identities and amounts of dietary polysaccharides directly impact the gut microbiota, determining which microorganisms consume specific nutrients is central for defining the relationship between diet and gut microbial ecology. Using a custom phenotyping array, we determined carbohydrate utilization profiles for 354 members of the Bacteroidetes, a dominant saccharolytic phylum. There was wide variation in the numbers and types of substrates degraded by individual bacteria, but phenotype-based clustering grouped members of the same species indicating that each species performs characteristic roles. The ability to utilize dietary polysaccharides and endogenous mucin glycans was negatively correlated, suggesting exclusion between these niches. By analyzing related Bacteroides ovatus/Bacteroides xylanisolvens strains that vary in their ability to utilize mucin glycans, we addressed whether gene clusters that confer this complex, multilocus trait are being gained or lost in individual strains. Pangenome reconstruction of these strains revealed a remarkably mosaic architecture in which genes involved in polysaccharide metabolism are highly variable and bioinformatics data provide evidence of interspecies gene transfer that might explain this genomic heterogeneity. Global transcriptomic analyses suggest that the ability to utilize mucin has been lost in some lineages of B. ovatus and B. xylanisolvens, which harbor residual gene clusters that are involved in mucin utilization by strains that still actively express this phenotype. Our data provide insight into the breadth and complexity of carbohydrate metabolism in the microbiome and the underlying genomic events that shape these behaviors.
