A Catalog of over 5,000 Metagenome-Assembled Microbial Genomes from the Caprinae Gut Microbiota

Zhang, Xiao-Xuan; Lv, Qingbo; Yan, Qiulong; Zhang, Yue; Guo, Ruochun; Meng, Jianghong; Ma, He; Qin, Siyuan; Zhu, Qinghe; Li, Chunqiu; Li, Rui; Liu, Gang; Li, Shenghui; Sun, Dongbo; Ni, Hong-Bo

doi:10.1128/spectrum.02211-22

Cited by 10 publications

(7 citation statements)

References 87 publications

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“…MAG sequences were interrogated using antiSMASH BGC detection software to determine whether Kyphosus gut-associated microbes might encode any unusual secondary metabolites. The majority of Bacillota , Bacteroidota , Verrucomicrobiota , and Gammaproteobacteria MAGs from both fish gut inocula and bioreactor enrichments encoded BGCs typical of taxonomic relatives found in other vertebrate gut environments, such as lanthipeptides, beta-lactones, and arylpolyenes ( 84 , 85 ). However, BGCs were not particularly abundant in our MAG catalog relative to other similar genomes.…”

Section: Resultsmentioning

confidence: 99%

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish

Oliver,

Podell,

Wegley Kelly

et al. 2024

mBio

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Coastal herbivorous fishes consume macroalgae, which is then degraded by microbes along their digestive tract. However, there is scarce genomic information about the microbiota that perform this degradation. This study explores the potential of Kyphosus gastrointestinal microbial symbionts to collaboratively degrade and ferment polysaccharides from red, green, and brown macroalgae through in silico study of carbohydrate-active enzyme and sulfatase sequences. Recovery of metagenome-assembled genomes (MAGs) from previously described Kyphosus gut metagenomes and newly sequenced bioreactor enrichments reveals differences in enzymatic capabilities between the major microbial taxa in Kyphosus guts. The most versatile of the recovered MAGs were from the Bacteroidota phylum, whose MAGs house enzyme collections able to decompose a variety of algal polysaccharides. Unique enzymes and predicted degradative capacities of genomes from the Bacillota (genus Vallitalea ) and Verrucomicrobiota (order Kiritimatiellales ) highlight the importance of metabolic contributions from multiple phyla to broaden polysaccharide degradation capabilities. Few genomes contain the required enzymes to fully degrade any complex sulfated algal polysaccharide alone. The distribution of suitable enzymes between MAGs originating from different taxa, along with the widespread detection of signal peptides in candidate enzymes, is consistent with cooperative extracellular degradation of these carbohydrates. This study leverages genomic evidence to reveal an untapped diversity at the enzyme and strain level among Kyphosus symbionts and their contributions to macroalgae decomposition. Bioreactor enrichments provide a genomic foundation for degradative and fermentative processes central to translating the knowledge gained from this system to the aquaculture and bioenergy sectors. IMPORTANCE Seaweed has long been considered a promising source of sustainable biomass for bioenergy and aquaculture feed, but scalable industrial methods for decomposing terrestrial compounds can struggle to break down seaweed polysaccharides efficiently due to their unique sulfated structures. Fish of the genus Kyphosus feed on seaweed by leveraging gastrointestinal bacteria to degrade algal polysaccharides into simple sugars. This study reconstructs metagenome-assembled genomes for these gastrointestinal bacteria to enhance our understanding of herbivorous fish digestion and fermentation of algal sugars. Investigations at the gene level identify Kyphosus guts as an untapped source of seaweed-degrading enzymes ripe for further characterization. These discoveries set the stage for future work incorporating marine enzymes and microbial communities in the industrial degradation of algal polysaccharides.

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Section: Resultsmentioning

confidence: 99%

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish

Oliver,

Podell,

Wegley Kelly

et al. 2024

mBio

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“…The bacterial abundance data came from a previously published study based on metagenomic sequencing ( 20 ). Potential interactions among families found in the gut microbiota (bacteria and archaea) and mycobiota were determined using Spearman correlations and corresponding network analysis, revealing 285 significant correlations in cross-family pairs in the gut.…”

Section: Resultsmentioning

confidence: 99%

“…Linear discriminant analysis (LDA) of the effect size (LEfSe) ( 42 ) was executed to identify the significant taxa that most likely explained the differences between groups, with a threshold LDA score of 2.0. Bacterial and fungal co-occurrence network analysis and visualization was performed by employing the Spearman method (rho cutoff = 0.5, P < 0.01) with packages psych (version 2.1.9) and igraph (version 1.2.6) in R and cytoscape software (version 3.7.2), and the bacterial abundance data were taken from the previous feces metagenomic shotgun sequencing data set ( 20 ) (Table S7 and S8).…”

Section: Methodsmentioning

confidence: 99%

Description of Gut Mycobiota Composition and Diversity of Caprinae Animals

Meng

et al. 2023

Microbiol Spectr

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In this study, we elucidated and analyzed the structure of the gut mycobiota of Caprinae animals from different regions. This study revealed differences in the structure of the gut mycobiota among Caprinae animals from different geographical environments. Based on previous findings, correlations between fungal and bacterial communities were analyzed. This study adds to previous research that has expanded the present understanding of the gut microbiome of Caprinae animals.

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“…MAG sequences were interrogated using antiSMASH biosynthetic gene cluster detection software to determine whether Kyphosus gut-associated microbial taxa might encode any unusual secondary metabolites. The majority of Bacillota , Bacteroidota , Verrucomicrobiota , and Gammaproteobacteria MAGs from both fish gut inocula and bioreactor enrichments encoded BGCs typical of taxonomic relatives found in other vertebrate gut environments, such as lanthipeptides, betalactone, and arylpolyene (81,82). However, BGCs were not particularly abundant in our MAG catalog relative to other similar genomes.…”

Section: Resultsmentioning

confidence: 99%

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides inKyphosusfish

Oliver,

Podell,

Kelly

et al. 2023

Preprint

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Coastal herbivorous fishes consume macroalgae, which is then degraded by microbes along their digestive tract. However, there is scarce foundational genomic work on the microbiota that perform this degradation. This study explores the potential ofKyphosusgastrointestinal microbial symbionts to collaboratively degrade and ferment polysaccharides from red, green, and brown macroalgae throughin silicostudy of carbohydrate-active enzyme and sulfatase sequences. Recovery of metagenome-assembled genomes (MAGs) reveals differences in enzymatic capabilities between the major microbial taxa inKyphosusguts. The most versatile of the recovered MAGs were from the Bacteroidota phylum, whose MAGs house enzymes able to decompose a variety of algal polysaccharides. Unique enzymes and predicted degradative capacities of genomes from theBacillota(genusVallitalea) andVerrucomicrobiota(order Kiritimatiellales) suggest the potential for microbial transfer between marine sediment andKyphosusdigestive tracts. Few genomes contain the required enzymes to fully degrade any complex sulfated algal polysaccharide alone. The distribution of suitable enzymes between MAGs originating from different taxa, along with the widespread detection of signal peptides in candidate enzymes, is consistent with cooperative extracellular degradation of these carbohydrates. This study leverages genomic evidence to reveal an untapped diversity at the enzyme and strain level amongKyphosussymbionts and their contributions to macroalgae decomposition. Bioreactor enrichments provide a genomic foundation for degradative and fermentative processes central to translating the knowledge gained from this system to the aquaculture and bioenergy sectors.ImportanceSeaweed has long been considered a promising source of sustainable biomass for bioenergy and aquaculture feed, but scalable industrial methods for decomposing terrestrial compounds can struggle to break down seaweed polysaccharides efficiently due to their unique sulfated structures. Fish of the genusKyphosusfeed on seaweed by leveraging gastrointestinal bacteria to degrade algal polysaccharides into simple sugars. This study is the first to build genomes for these gastrointestinal bacteria to enhance our understanding of herbivorous fish digestion and fermentation of algal sugars. Investigations at the gene level identifyKyphosusguts as an untapped source of seaweed-degrading enzymes ripe for further characterization. These discoveries set the stage for future work incorporating marine enzymes and microbial communities in the industrial degradation of algal polysaccharides.

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A Catalog of over 5,000 Metagenome-Assembled Microbial Genomes from the Caprinae Gut Microbiota

Abstract: We constructed a microbiota catalog containing 5,046 MAGs from Caprinae gut from six regions of China. Most of the MAGs do not overlap known databases and appear to be potentially new species.

Cited by 10 publications

References 87 publications

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish

Description of Gut Mycobiota Composition and Diversity of Caprinae Animals

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides inKyphosusfish

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