Large-Scale Metagenome Assembly Reveals Novel Animal-Associated Microbial Genomes, Biosynthetic Gene Clusters, and Other Genetic Diversity

ABSTRACT Large-scale metagenome assemblies of human microbiomes have produced a vast catalogue of previously unseen microbial genomes; however, comparatively few microbial genomes derive from other vertebrates. Here, we generated 5,596 metagenome-assembled genomes (MAGs) from the gut metagenomes of...

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Autores principales:	Nicholas D. Youngblut, Jacobo de la Cuesta-Zuluaga, Georg H. Reischer, Silke Dauser, Nathalie Schuster, Chris Walzer, Gabrielle Stalder, Andreas H. Farnleitner, Ruth E. Ley
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	animal microbiome gut metagenome assembly novel diversity antimicrobial resistance biosynthetic gene cluster Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a9948b5f78ca42d1a6e8e52068bbc29d
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spelling	oai:doaj.org-article:a9948b5f78ca42d1a6e8e52068bbc29d2021-12-02T19:47:38ZLarge-Scale Metagenome Assembly Reveals Novel Animal-Associated Microbial Genomes, Biosynthetic Gene Clusters, and Other Genetic Diversity10.1128/mSystems.01045-202379-5077https://doaj.org/article/a9948b5f78ca42d1a6e8e52068bbc29d2020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01045-20https://doaj.org/toc/2379-5077ABSTRACT Large-scale metagenome assemblies of human microbiomes have produced a vast catalogue of previously unseen microbial genomes; however, comparatively few microbial genomes derive from other vertebrates. Here, we generated 5,596 metagenome-assembled genomes (MAGs) from the gut metagenomes of 180 predominantly wild animal species representing 5 classes, in addition to 14 existing animal gut metagenome data sets. The MAGs comprised 1,522 species-level genome bins (SGBs), most of which were novel at the species, genus, or family level, and the majority were enriched in host versus environment metagenomes. Many traits distinguished SGBs enriched in host or environmental biomes, including the number of antimicrobial resistance genes. We identified 1,986 diverse biosynthetic gene clusters; only 23 clustered with any MIBiG database references. Gene-based assembly revealed tremendous gene diversity, much of it host or environment specific. Our MAG and gene data sets greatly expand the microbial genome repertoire and provide a broad view of microbial adaptations to the vertebrate gut. IMPORTANCE Microbiome studies on a select few mammalian species (e.g., humans, mice, and cattle) have revealed a great deal of novel genomic diversity in the gut microbiome. However, little is known of the microbial diversity in the gut of other vertebrates. We studied the gut microbiomes of a large set of mostly wild animal species consisting of mammals, birds, reptiles, amphibians, and fish. Unfortunately, we found that existing reference databases commonly used for metagenomic analyses failed to capture the microbiome diversity among vertebrates. To increase database representation, we applied advanced metagenome assembly methods to our animal gut data and to many public gut metagenome data sets that had not been used to obtain microbial genomes. Our resulting genome and gene cluster collections comprised a great deal of novel taxonomic and genomic diversity, which we extensively characterized. Our findings substantially expand what is known of microbial genomic diversity in the vertebrate gut.Nicholas D. YoungblutJacobo de la Cuesta-ZuluagaGeorg H. ReischerSilke DauserNathalie SchusterChris WalzerGabrielle StalderAndreas H. FarnleitnerRuth E. LeyAmerican Society for Microbiologyarticleanimal microbiomegutmetagenome assemblynovel diversityantimicrobial resistancebiosynthetic gene clusterMicrobiologyQR1-502ENmSystems, Vol 5, Iss 6 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	animal microbiome gut metagenome assembly novel diversity antimicrobial resistance biosynthetic gene cluster Microbiology QR1-502
spellingShingle	animal microbiome gut metagenome assembly novel diversity antimicrobial resistance biosynthetic gene cluster Microbiology QR1-502 Nicholas D. Youngblut Jacobo de la Cuesta-Zuluaga Georg H. Reischer Silke Dauser Nathalie Schuster Chris Walzer Gabrielle Stalder Andreas H. Farnleitner Ruth E. Ley Large-Scale Metagenome Assembly Reveals Novel Animal-Associated Microbial Genomes, Biosynthetic Gene Clusters, and Other Genetic Diversity
description	ABSTRACT Large-scale metagenome assemblies of human microbiomes have produced a vast catalogue of previously unseen microbial genomes; however, comparatively few microbial genomes derive from other vertebrates. Here, we generated 5,596 metagenome-assembled genomes (MAGs) from the gut metagenomes of 180 predominantly wild animal species representing 5 classes, in addition to 14 existing animal gut metagenome data sets. The MAGs comprised 1,522 species-level genome bins (SGBs), most of which were novel at the species, genus, or family level, and the majority were enriched in host versus environment metagenomes. Many traits distinguished SGBs enriched in host or environmental biomes, including the number of antimicrobial resistance genes. We identified 1,986 diverse biosynthetic gene clusters; only 23 clustered with any MIBiG database references. Gene-based assembly revealed tremendous gene diversity, much of it host or environment specific. Our MAG and gene data sets greatly expand the microbial genome repertoire and provide a broad view of microbial adaptations to the vertebrate gut. IMPORTANCE Microbiome studies on a select few mammalian species (e.g., humans, mice, and cattle) have revealed a great deal of novel genomic diversity in the gut microbiome. However, little is known of the microbial diversity in the gut of other vertebrates. We studied the gut microbiomes of a large set of mostly wild animal species consisting of mammals, birds, reptiles, amphibians, and fish. Unfortunately, we found that existing reference databases commonly used for metagenomic analyses failed to capture the microbiome diversity among vertebrates. To increase database representation, we applied advanced metagenome assembly methods to our animal gut data and to many public gut metagenome data sets that had not been used to obtain microbial genomes. Our resulting genome and gene cluster collections comprised a great deal of novel taxonomic and genomic diversity, which we extensively characterized. Our findings substantially expand what is known of microbial genomic diversity in the vertebrate gut.
format	article
author	Nicholas D. Youngblut Jacobo de la Cuesta-Zuluaga Georg H. Reischer Silke Dauser Nathalie Schuster Chris Walzer Gabrielle Stalder Andreas H. Farnleitner Ruth E. Ley
author_facet	Nicholas D. Youngblut Jacobo de la Cuesta-Zuluaga Georg H. Reischer Silke Dauser Nathalie Schuster Chris Walzer Gabrielle Stalder Andreas H. Farnleitner Ruth E. Ley
author_sort	Nicholas D. Youngblut
title	Large-Scale Metagenome Assembly Reveals Novel Animal-Associated Microbial Genomes, Biosynthetic Gene Clusters, and Other Genetic Diversity
title_short	Large-Scale Metagenome Assembly Reveals Novel Animal-Associated Microbial Genomes, Biosynthetic Gene Clusters, and Other Genetic Diversity
title_full	Large-Scale Metagenome Assembly Reveals Novel Animal-Associated Microbial Genomes, Biosynthetic Gene Clusters, and Other Genetic Diversity
title_fullStr	Large-Scale Metagenome Assembly Reveals Novel Animal-Associated Microbial Genomes, Biosynthetic Gene Clusters, and Other Genetic Diversity
title_full_unstemmed	Large-Scale Metagenome Assembly Reveals Novel Animal-Associated Microbial Genomes, Biosynthetic Gene Clusters, and Other Genetic Diversity
title_sort	large-scale metagenome assembly reveals novel animal-associated microbial genomes, biosynthetic gene clusters, and other genetic diversity
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/a9948b5f78ca42d1a6e8e52068bbc29d
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Large-Scale Metagenome Assembly Reveals Novel Animal-Associated Microbial Genomes, Biosynthetic Gene Clusters, and Other Genetic Diversity

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