Micronutrient Requirements and Sharing Capabilities of the Human Gut Microbiome
The human gut microbiome harbors a diverse array of metabolic pathways contributing to its development and homeostasis via a complex web of diet-dependent metabolic interactions within the microbial community and host. Genomics-based reconstruction and predictive modeling of these interactions would...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-06-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.01316/full |
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| author | Dmitry A. Rodionov Dmitry A. Rodionov Aleksandr A. Arzamasov Aleksandr A. Arzamasov Matvei S. Khoroshkin Stanislav N. Iablokov Stanislav N. Iablokov Semen A. Leyn Semen A. Leyn Scott N. Peterson Pavel S. Novichkov Andrei L. Osterman |
| author_facet | Dmitry A. Rodionov Dmitry A. Rodionov Aleksandr A. Arzamasov Aleksandr A. Arzamasov Matvei S. Khoroshkin Stanislav N. Iablokov Stanislav N. Iablokov Semen A. Leyn Semen A. Leyn Scott N. Peterson Pavel S. Novichkov Andrei L. Osterman |
| author_sort | Dmitry A. Rodionov |
| collection | DOAJ |
| description | The human gut microbiome harbors a diverse array of metabolic pathways contributing to its development and homeostasis via a complex web of diet-dependent metabolic interactions within the microbial community and host. Genomics-based reconstruction and predictive modeling of these interactions would provide a framework for diagnostics and treatment of dysbiosis-related syndromes via rational selection of therapeutic prebiotics and dietary nutrients. Of particular interest are micronutrients, such as B-group vitamins, precursors of indispensable metabolic cofactors, that are produced de novo by some gut bacteria (prototrophs) but must be provided exogenously in the diet for many other bacterial species (auxotrophs) as well as for the mammalian host. Cross-feeding of B vitamins between prototrophic and auxotrophic species is expected to strongly contribute to the homeostasis of microbial communities in the distal gut given the efficient absorption of dietary vitamins in the upper gastrointestinal tract. To confidently estimate the balance of microbiome micronutrient biosynthetic capabilities and requirements using available genomic data, we have performed a subsystems-based reconstruction of biogenesis, salvage and uptake for eight B vitamins (B1, B2, B3, B5, B6, B7, B9, and B12) and queuosine (essential factor in tRNA modification) over a reference set of 2,228 bacterial genomes representing 690 cultured species of the human gastrointestinal microbiota. This allowed us to classify the studied organisms with respect to their pathway variants and infer their prototrophic vs. auxotrophic phenotypes. In addition to canonical vitamin pathways, several conserved partial pathways were identified pointing to alternative routes of syntrophic metabolism and expanding a microbial vitamin “menu” by several pathway intermediates (vitamers) such as thiazole, quinolinate, dethiobiotin, pantoate. A cross-species comparison was applied to assess the extent of conservation of vitamin phenotypes at distinct taxonomic levels (from strains to families). The obtained reference collection combined with 16S rRNA gene-based phylogenetic profiles was used to deduce phenotype profiles of the human gut microbiota across in two large cohorts. This analysis provided the first estimate of B-vitamin requirements, production and sharing capabilities in the human gut microbiome establishing predictive phenotype profiling as a new approach to classification of microbiome samples. Future expansion of our reference genomic collection of metabolic phenotypes will allow further improvement in coverage and accuracy of predictive phenotype profiling of the human microbiome. |
| first_indexed | 2024-12-21T13:29:25Z |
| format | Article |
| id | doaj.art-f1e94e29d1064d9882604bbadaca3f70 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-21T13:29:25Z |
| publishDate | 2019-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-f1e94e29d1064d9882604bbadaca3f702022-12-21T19:02:21ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-06-011010.3389/fmicb.2019.01316447195Micronutrient Requirements and Sharing Capabilities of the Human Gut MicrobiomeDmitry A. Rodionov0Dmitry A. Rodionov1Aleksandr A. Arzamasov2Aleksandr A. Arzamasov3Matvei S. Khoroshkin4Stanislav N. Iablokov5Stanislav N. Iablokov6Semen A. Leyn7Semen A. Leyn8Scott N. Peterson9Pavel S. Novichkov10Andrei L. Osterman11Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesA.A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, RussiaSanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesA.A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, RussiaA.A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, RussiaA.A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, RussiaDepartment of Physics, P.G. Demidov Yaroslavl State University, Yaroslavl, RussiaSanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesA.A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, RussiaSanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesLawrence Berkeley National Laboratory, Berkeley, CA, United StatesSanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesThe human gut microbiome harbors a diverse array of metabolic pathways contributing to its development and homeostasis via a complex web of diet-dependent metabolic interactions within the microbial community and host. Genomics-based reconstruction and predictive modeling of these interactions would provide a framework for diagnostics and treatment of dysbiosis-related syndromes via rational selection of therapeutic prebiotics and dietary nutrients. Of particular interest are micronutrients, such as B-group vitamins, precursors of indispensable metabolic cofactors, that are produced de novo by some gut bacteria (prototrophs) but must be provided exogenously in the diet for many other bacterial species (auxotrophs) as well as for the mammalian host. Cross-feeding of B vitamins between prototrophic and auxotrophic species is expected to strongly contribute to the homeostasis of microbial communities in the distal gut given the efficient absorption of dietary vitamins in the upper gastrointestinal tract. To confidently estimate the balance of microbiome micronutrient biosynthetic capabilities and requirements using available genomic data, we have performed a subsystems-based reconstruction of biogenesis, salvage and uptake for eight B vitamins (B1, B2, B3, B5, B6, B7, B9, and B12) and queuosine (essential factor in tRNA modification) over a reference set of 2,228 bacterial genomes representing 690 cultured species of the human gastrointestinal microbiota. This allowed us to classify the studied organisms with respect to their pathway variants and infer their prototrophic vs. auxotrophic phenotypes. In addition to canonical vitamin pathways, several conserved partial pathways were identified pointing to alternative routes of syntrophic metabolism and expanding a microbial vitamin “menu” by several pathway intermediates (vitamers) such as thiazole, quinolinate, dethiobiotin, pantoate. A cross-species comparison was applied to assess the extent of conservation of vitamin phenotypes at distinct taxonomic levels (from strains to families). The obtained reference collection combined with 16S rRNA gene-based phylogenetic profiles was used to deduce phenotype profiles of the human gut microbiota across in two large cohorts. This analysis provided the first estimate of B-vitamin requirements, production and sharing capabilities in the human gut microbiome establishing predictive phenotype profiling as a new approach to classification of microbiome samples. Future expansion of our reference genomic collection of metabolic phenotypes will allow further improvement in coverage and accuracy of predictive phenotype profiling of the human microbiome.https://www.frontiersin.org/article/10.3389/fmicb.2019.01316/fullgut microbiomevitamin metabolismmetagenomics16Scomparative genomics |
| spellingShingle | Dmitry A. Rodionov Dmitry A. Rodionov Aleksandr A. Arzamasov Aleksandr A. Arzamasov Matvei S. Khoroshkin Stanislav N. Iablokov Stanislav N. Iablokov Semen A. Leyn Semen A. Leyn Scott N. Peterson Pavel S. Novichkov Andrei L. Osterman Micronutrient Requirements and Sharing Capabilities of the Human Gut Microbiome Frontiers in Microbiology gut microbiome vitamin metabolism metagenomics 16S comparative genomics |
| title | Micronutrient Requirements and Sharing Capabilities of the Human Gut Microbiome |
| title_full | Micronutrient Requirements and Sharing Capabilities of the Human Gut Microbiome |
| title_fullStr | Micronutrient Requirements and Sharing Capabilities of the Human Gut Microbiome |
| title_full_unstemmed | Micronutrient Requirements and Sharing Capabilities of the Human Gut Microbiome |
| title_short | Micronutrient Requirements and Sharing Capabilities of the Human Gut Microbiome |
| title_sort | micronutrient requirements and sharing capabilities of the human gut microbiome |
| topic | gut microbiome vitamin metabolism metagenomics 16S comparative genomics |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.01316/full |
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