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The genomic landscape of reference genomes of cultivated human gut bacteria.

ABSTRACT: Culture-independent metagenomic studies have revolutionized our understanding of the gut microbiota. However, the lack of full genomes from cultured species is still a limitation for in-depth studies of the gut microbiota. Here we present a substantially expanded version of our Cultivated Genome Reference (CGR), termed CGR2, providing 3324 high-quality draft genomes from isolates selected from a large-scale cultivation of bacterial isolates from fecal samples of healthy Chinese individuals. The CGR2 classifies 527 species (179 previously unidentified species) from 8 phyla, and uncovers a genomic and functional diversity of Collinsella aerofaciens. The CGR2 genomes match 126 metagenome-assembled genomes without cultured representatives in the Unified Human Gastrointestinal Genome (UHGG) collection and harbor 3767 unidentified secondary metabolite biosynthetic gene clusters, providing a source of natural compounds with pharmaceutical potentials. We uncover accurate phage-bacterium linkages providing information on the evolutionary characteristics of interaction between bacteriophages and bacteria at the strain level.

SUBMITTER: Lin X

PROVIDER: S-EPMC10039858 | biostudies-literature | 2023 Mar

REPOSITORIES: biostudies-literature

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The genomic landscape of reference genomes of cultivated human gut bacteria.

Lin Xiaoqian X Hu Tongyuan T Chen Jianwei J Liang Hewei H Zhou Jianwei J Wu Zhinan Z Ye Chen C Jin Xin X Xu Xun X Zhang Wenwei W Jing Xiaohuan X Yang Tao T Wang Jian J Yang Huanming H Kristiansen Karsten K Xiao Liang L Zou Yuanqiang Y

Nature communications 20230325 1

Culture-independent metagenomic studies have revolutionized our understanding of the gut microbiota. However, the lack of full genomes from cultured species is still a limitation for in-depth studies of the gut microbiota. Here we present a substantially expanded version of our Cultivated Genome Reference (CGR), termed CGR2, providing 3324 high-quality draft genomes from isolates selected from a large-scale cultivation of bacterial isolates from fecal samples of healthy Chinese individuals. The ...[more]

PMID: 36966151

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Project description:BackgroundMetagenome sampling bias for geographical location and lifestyle is partially responsible for the incomplete catalog of reference genomes of gut microbial species. Thus, genome assembly from currently under-represented populations may effectively expand the reference gut microbiome and improve taxonomic and functional profiling.MethodsWe assembled genomes using public whole-metagenomic shotgun sequencing (WMS) data for 110 and 645 fecal samples from India and Japan, respectively. In addition, we assembled genomes from newly generated WMS data for 90 fecal samples collected from Korea. Expecting genome assembly for low-abundance species may require a much deeper sequencing than that usually employed, so we performed ultra-deep WMS (> 30 Gbp or > 100 million read pairs) for the fecal samples from Korea. We consequently assembled 29,082 prokaryotic genomes from 845 fecal metagenomes for the three under-represented Asian countries and combined them with the Unified Human Gastrointestinal Genome (UHGG) to generate an expanded catalog, the Human Reference Gut Microbiome (HRGM).ResultsHRGM contains 232,098 non-redundant genomes for 5414 representative prokaryotic species including 780 that are novel, > 103 million unique proteins, and > 274 million single-nucleotide variants. This is an over 10% increase from the UHGG. The new 780 species were enriched for the Bacteroidaceae family, including species associated with high-fiber and seaweed-rich diets. Single-nucleotide variant density was positively associated with the speciation rate of gut commensals. We found that ultra-deep sequencing facilitated the assembly of genomes for low-abundance taxa, and deep sequencing (e.g., > 20 million read pairs) may be needed for the profiling of low-abundance taxa. Importantly, the HRGM significantly improved the taxonomic and functional classification of sequencing reads from fecal samples. Finally, analysis of human self-antigen homologs on the HRGM species genomes suggested that bacterial taxa with high cross-reactivity potential may contribute more to the pathogenesis of gut microbiome-associated diseases than those with low cross-reactivity potential by promoting inflammatory condition.ConclusionsBy including gut metagenomes from previously under-represented Asian countries, Korea, India, and Japan, we developed a substantially expanded microbiome catalog, HRGM. Information of the microbial genomes and coding genes is publicly available ( www.mbiomenet.org/HRGM/ ). HRGM will facilitate the identification and functional analysis of disease-associated gut microbiota.

Project description: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. IMPORTANCE Nonharmful bacteria are the primary microbial symbionts that inhabit the human gastrointestinal tract. These bacteria play many beneficial roles and in some cases can modify disease states, making it important to understand which nutrients sustain specific lineages. This knowledge will in turn lead to strategies to intentionally manipulate the gut microbial ecosystem. We designed a scalable, high-throughput platform for measuring the ability of gut bacteria to utilize polysaccharides, of which many are derived from dietary fiber sources that can be manipulated easily. Our results provide paths to expand phenotypic surveys of more diverse gut bacteria to understand their functions and also to leverage dietary fibers to alter the physiology of the gut microbial community.

Dataset Information

The genomic landscape of reference genomes of cultivated human gut bacteria.

Publications

The genomic landscape of reference genomes of cultivated human gut bacteria.

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