Cultivation-independent genomes greatly expand taxonomic-profiling capabilities of mOTUs across various environments
Abstract Background Taxonomic profiling is a fundamental task in microbiome research that aims to detect and quantify the relative abundance of microorganisms in biological samples. Available methods using shotgun metagenomic data generally depend on the deposition of sequenced and taxonomically ann...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2022-12-01
|
| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-022-01410-z |
| _version_ | 1811179134429167616 |
|---|---|
| author | Hans-Joachim Ruscheweyh Alessio Milanese Lucas Paoli Nicolai Karcher Quentin Clayssen Marisa Isabell Keller Jakob Wirbel Peer Bork Daniel R. Mende Georg Zeller Shinichi Sunagawa |
| author_facet | Hans-Joachim Ruscheweyh Alessio Milanese Lucas Paoli Nicolai Karcher Quentin Clayssen Marisa Isabell Keller Jakob Wirbel Peer Bork Daniel R. Mende Georg Zeller Shinichi Sunagawa |
| author_sort | Hans-Joachim Ruscheweyh |
| collection | DOAJ |
| description | Abstract Background Taxonomic profiling is a fundamental task in microbiome research that aims to detect and quantify the relative abundance of microorganisms in biological samples. Available methods using shotgun metagenomic data generally depend on the deposition of sequenced and taxonomically annotated genomes, usually from cultures of isolated strains, in reference databases (reference genomes). However, the majority of microorganisms have not been cultured yet. Thus, a substantial fraction of microbial community members remains unaccounted for during taxonomic profiling, particularly in samples from underexplored environments. To address this issue, we developed the mOTU profiler, a tool that enables reference genome-independent species-level profiling of metagenomes. As such, it supports the identification and quantification of both “known” and “unknown” species based on a set of select marker genes. Results We present mOTUs3, a command line tool that enables the profiling of metagenomes for >33,000 species-level operational taxonomic units. To achieve this, we leveraged the reconstruction of >600,000 draft genomes, most of which are metagenome-assembled genomes (MAGs), from diverse microbiomes, including soil, freshwater systems, and the gastrointestinal tract of ruminants and other animals, which we found to be underrepresented by reference genomes. Overall, two thirds of all species-level taxa lacked a reference genome. The cumulative relative abundance of these newly included taxa was low in well-studied microbiomes, such as the human body sites (6–11%). By contrast, they accounted for substantial proportions (ocean, freshwater, soil: 43–63%) or even the majority (pig, fish, cattle: 60–80%) of the relative abundance across diverse non-human-associated microbiomes. Using community-developed benchmarks and datasets, we found mOTUs3 to be more accurate than other methods and to be more congruent with 16S rRNA gene-based methods for taxonomic profiling. Furthermore, we demonstrate that mOTUs3 increases the resolution of well-known microbial groups into species-level taxa and helps identify new differentially abundant taxa in comparative metagenomic studies. Conclusions We developed mOTUs3 to enable accurate species-level profiling of metagenomes. Compared to other methods, it provides a more comprehensive view of prokaryotic community diversity, in particular for currently underexplored microbiomes. To facilitate comparative analyses by the research community, it is released with >11,000 precomputed profiles for publicly available metagenomes and is freely available at: https://github.com/motu-tool/mOTUs . Video Abstract |
| first_indexed | 2024-04-11T06:30:42Z |
| format | Article |
| id | doaj.art-7dcca887fbe548e4aa354361f2fc4c09 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-11T06:30:42Z |
| publishDate | 2022-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-7dcca887fbe548e4aa354361f2fc4c092022-12-22T04:40:08ZengBMCMicrobiome2049-26182022-12-0110111210.1186/s40168-022-01410-zCultivation-independent genomes greatly expand taxonomic-profiling capabilities of mOTUs across various environmentsHans-Joachim Ruscheweyh0Alessio Milanese1Lucas Paoli2Nicolai Karcher3Quentin Clayssen4Marisa Isabell Keller5Jakob Wirbel6Peer Bork7Daniel R. Mende8Georg Zeller9Shinichi Sunagawa10Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH ZürichDepartment of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH ZürichDepartment of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH ZürichStructural and Computational Biology Unit, European Molecular Biology LaboratoryDepartment of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH ZürichStructural and Computational Biology Unit, European Molecular Biology LaboratoryStructural and Computational Biology Unit, European Molecular Biology LaboratoryStructural and Computational Biology Unit, European Molecular Biology LaboratoryDepartment of Medical Microbiology, Amsterdam UMC, University of AmsterdamStructural and Computational Biology Unit, European Molecular Biology LaboratoryDepartment of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH ZürichAbstract Background Taxonomic profiling is a fundamental task in microbiome research that aims to detect and quantify the relative abundance of microorganisms in biological samples. Available methods using shotgun metagenomic data generally depend on the deposition of sequenced and taxonomically annotated genomes, usually from cultures of isolated strains, in reference databases (reference genomes). However, the majority of microorganisms have not been cultured yet. Thus, a substantial fraction of microbial community members remains unaccounted for during taxonomic profiling, particularly in samples from underexplored environments. To address this issue, we developed the mOTU profiler, a tool that enables reference genome-independent species-level profiling of metagenomes. As such, it supports the identification and quantification of both “known” and “unknown” species based on a set of select marker genes. Results We present mOTUs3, a command line tool that enables the profiling of metagenomes for >33,000 species-level operational taxonomic units. To achieve this, we leveraged the reconstruction of >600,000 draft genomes, most of which are metagenome-assembled genomes (MAGs), from diverse microbiomes, including soil, freshwater systems, and the gastrointestinal tract of ruminants and other animals, which we found to be underrepresented by reference genomes. Overall, two thirds of all species-level taxa lacked a reference genome. The cumulative relative abundance of these newly included taxa was low in well-studied microbiomes, such as the human body sites (6–11%). By contrast, they accounted for substantial proportions (ocean, freshwater, soil: 43–63%) or even the majority (pig, fish, cattle: 60–80%) of the relative abundance across diverse non-human-associated microbiomes. Using community-developed benchmarks and datasets, we found mOTUs3 to be more accurate than other methods and to be more congruent with 16S rRNA gene-based methods for taxonomic profiling. Furthermore, we demonstrate that mOTUs3 increases the resolution of well-known microbial groups into species-level taxa and helps identify new differentially abundant taxa in comparative metagenomic studies. Conclusions We developed mOTUs3 to enable accurate species-level profiling of metagenomes. Compared to other methods, it provides a more comprehensive view of prokaryotic community diversity, in particular for currently underexplored microbiomes. To facilitate comparative analyses by the research community, it is released with >11,000 precomputed profiles for publicly available metagenomes and is freely available at: https://github.com/motu-tool/mOTUs . Video Abstracthttps://doi.org/10.1186/s40168-022-01410-zMetagenomicsMicrobial communityBenchmarkingTaxonomic profilingMarker geneMetagenome-assembled genome |
| spellingShingle | Hans-Joachim Ruscheweyh Alessio Milanese Lucas Paoli Nicolai Karcher Quentin Clayssen Marisa Isabell Keller Jakob Wirbel Peer Bork Daniel R. Mende Georg Zeller Shinichi Sunagawa Cultivation-independent genomes greatly expand taxonomic-profiling capabilities of mOTUs across various environments Microbiome Metagenomics Microbial community Benchmarking Taxonomic profiling Marker gene Metagenome-assembled genome |
| title | Cultivation-independent genomes greatly expand taxonomic-profiling capabilities of mOTUs across various environments |
| title_full | Cultivation-independent genomes greatly expand taxonomic-profiling capabilities of mOTUs across various environments |
| title_fullStr | Cultivation-independent genomes greatly expand taxonomic-profiling capabilities of mOTUs across various environments |
| title_full_unstemmed | Cultivation-independent genomes greatly expand taxonomic-profiling capabilities of mOTUs across various environments |
| title_short | Cultivation-independent genomes greatly expand taxonomic-profiling capabilities of mOTUs across various environments |
| title_sort | cultivation independent genomes greatly expand taxonomic profiling capabilities of motus across various environments |
| topic | Metagenomics Microbial community Benchmarking Taxonomic profiling Marker gene Metagenome-assembled genome |
| url | https://doi.org/10.1186/s40168-022-01410-z |
| work_keys_str_mv | AT hansjoachimruscheweyh cultivationindependentgenomesgreatlyexpandtaxonomicprofilingcapabilitiesofmotusacrossvariousenvironments AT alessiomilanese cultivationindependentgenomesgreatlyexpandtaxonomicprofilingcapabilitiesofmotusacrossvariousenvironments AT lucaspaoli cultivationindependentgenomesgreatlyexpandtaxonomicprofilingcapabilitiesofmotusacrossvariousenvironments AT nicolaikarcher cultivationindependentgenomesgreatlyexpandtaxonomicprofilingcapabilitiesofmotusacrossvariousenvironments AT quentinclayssen cultivationindependentgenomesgreatlyexpandtaxonomicprofilingcapabilitiesofmotusacrossvariousenvironments AT marisaisabellkeller cultivationindependentgenomesgreatlyexpandtaxonomicprofilingcapabilitiesofmotusacrossvariousenvironments AT jakobwirbel cultivationindependentgenomesgreatlyexpandtaxonomicprofilingcapabilitiesofmotusacrossvariousenvironments AT peerbork cultivationindependentgenomesgreatlyexpandtaxonomicprofilingcapabilitiesofmotusacrossvariousenvironments AT danielrmende cultivationindependentgenomesgreatlyexpandtaxonomicprofilingcapabilitiesofmotusacrossvariousenvironments AT georgzeller cultivationindependentgenomesgreatlyexpandtaxonomicprofilingcapabilitiesofmotusacrossvariousenvironments AT shinichisunagawa cultivationindependentgenomesgreatlyexpandtaxonomicprofilingcapabilitiesofmotusacrossvariousenvironments |