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Genomic insights from Monoglobus pectinilyticus: a pectin-degrading specialist bacterium in the human colon.

ABSTRACT: Pectin is abundant in modern day diets, as it comprises the middle lamellae and one-third of the dry carbohydrate weight of fruit and vegetable cell walls. Currently there is no specialized model organism for studying pectin fermentation in the human colon, as our collective understanding is informed by versatile glycan-degrading bacteria rather than by specialist pectin degraders. Here we show that the genome of Monoglobus pectinilyticus possesses a highly specialized glycobiome for pectin degradation, unique amongst Firmicutes known to be in the human gut. Its genome encodes a simple set of metabolic pathways relevant to pectin sugar utilization, and its predicted glycobiome comprises an unusual distribution of carbohydrate-active enzymes (CAZymes) with numerous extracellular methyl/acetyl esterases and pectate lyases. We predict the M. pectinilyticus degradative process is facilitated by cell-surface S-layer homology (SLH) domain-containing proteins, which proteomics analysis shows are differentially expressed in response to pectin. Some of these abundant cell surface proteins of M. pectinilyticus share unique modular organizations rarely observed in human gut bacteria, featuring pectin-specific CAZyme domains and the cell wall-anchoring SLH motifs. We observed M. pectinilyticus degrades various pectins, RG-I, and galactan to produce polysaccharide degradation products (PDPs) which are presumably shared with other inhabitants of the human gut microbiome (HGM). This strain occupies a new ecological niche for a primary degrader specialized in foraging a habitually consumed plant glycan, thereby enriching our understanding of the diverse community profile of the HGM.

SUBMITTER: Kim CC

PROVIDER: S-EPMC6776006 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Chryseobacterium spp. are Gram-negative rods found ubiquitously in the environment, with certain species being reported as having unusual degrading properties. Polyvinyl alcohol (PVA) is used widely in industry but causes serious global environmental pollution. Here, we report the complete genome sequence of a novel bacterium, AC3, that efficiently degrades PVA. As the representative genome of Chryseobacterium nepalense, key genomic characteristics (e.g., mobile genetic elements, horizontal genes, genome-scale metabolic network, secondary metabolite biosynthesis gene clusters, and carbohydrate-active enzymes) were comprehensively investigated to reveal the potential genetic features of this species. Core genome phylogenetic analysis in combination with average nucleotide identity, average amino acid identity, and in silico DNA-DNA hybridization values provided an accurate taxonomic position of C. nepalense in the genus Chryseobacterium. Comparative genomic analysis of AC3 with closely related species suggested evolutionary dynamics characterized by a species-specific genetic repertoire, dramatic rearrangements, and evolutionary constraints driven by selective pressure, which facilitated the speciation and adaptative evolution of C. nepalense. Biogeographic characterization indicated that this species is ubiquitously distributed not only in soil habitats but also in a variety of other source niches. Bioinformatic analysis revealed the potential genetic basis of PVA degradation in AC3, which included six putative genes associated with the synthesis of PVA dehydrogenase, cytochrome c, oxidized PVA hydrolase, and secondary alcohol dehydrogenase. Our study reports the first complete genome of C. nepalense with PVA-degrading properties, providing comprehensive insights into the genomic characteristics of this species and increasing our understanding of the microbial degradation of PVA. IMPORTANCE Although PVA is a biodegradable polymer, the widespread use of PVA in global industrialization has resulted in serious environmental problems. To date, knowledge of effective and applicable PVA-degrading bacteria is limited, and thus, the discovery of novel PVA biodegraders is pertinent. Here, we isolated a novel bacterial strain, AC3, which efficiently degraded PVA. The complete genome of AC3 was sequenced as the first genome sequence of the species C. nepalense. Comparative genomic analysis was performed to comprehensively investigate the phylogenetic relationships, genome-scale metabolic network, key genomic characteristics associated with genomic evolution, evolutionary dynamics between AC3 and its close relatives, and biogeographic characterization of C. nepalense, particularly regarding the potential genetic basis of PVA degradation. These findings could advance our understanding of the genomic characteristics of C. nepalense and PVA bioremediation.

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Genomic insights from Monoglobus pectinilyticus: a pectin-degrading specialist bacterium in the human colon.

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