Vitamin interdependencies predicted by metagenomics-informed network analyses and validated in microbial community microcosms
Abstract Metagenomic or metabarcoding data are often used to predict microbial interactions in complex communities, but these predictions are rarely explored experimentally. Here, we use an organism abundance correlation network to investigate factors that control community organization in mine tail...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-08-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-40360-4 |
| _version_ | 1797558316202721280 |
|---|---|
| author | Tomas Hessler Robert J. Huddy Rohan Sachdeva Shufei Lei Susan T. L. Harrison Spencer Diamond Jillian F. Banfield |
| author_facet | Tomas Hessler Robert J. Huddy Rohan Sachdeva Shufei Lei Susan T. L. Harrison Spencer Diamond Jillian F. Banfield |
| author_sort | Tomas Hessler |
| collection | DOAJ |
| description | Abstract Metagenomic or metabarcoding data are often used to predict microbial interactions in complex communities, but these predictions are rarely explored experimentally. Here, we use an organism abundance correlation network to investigate factors that control community organization in mine tailings-derived laboratory microbial consortia grown under dozens of conditions. The network is overlaid with metagenomic information about functional capacities to generate testable hypotheses. We develop a metric to predict the importance of each node within its local network environments relative to correlated vitamin auxotrophs, and predict that a Variovorax species is a hub as an important source of thiamine. Quantification of thiamine during the growth of Variovorax in minimal media show high levels of thiamine production, up to 100 mg/L. A few of the correlated thiamine auxotrophs are predicted to produce pantothenate, which we show is required for growth of Variovorax, supporting that a subset of vitamin-dependent interactions are mutualistic. A Cryptococcus yeast produces the B-vitamin pantothenate, and co-culturing with Variovorax leads to a 90-130-fold fitness increase for both organisms. Our study demonstrates the predictive power of metagenome-informed, microbial consortia-based network analyses for identifying microbial interactions that underpin the structure and functioning of microbial communities. |
| first_indexed | 2024-03-10T17:29:46Z |
| format | Article |
| id | doaj.art-7d2f93f7bbd141dc8c8af112c5549cbb |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-10T17:29:46Z |
| publishDate | 2023-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-7d2f93f7bbd141dc8c8af112c5549cbb2023-11-20T10:04:39ZengNature PortfolioNature Communications2041-17232023-08-0114111210.1038/s41467-023-40360-4Vitamin interdependencies predicted by metagenomics-informed network analyses and validated in microbial community microcosmsTomas Hessler0Robert J. Huddy1Rohan Sachdeva2Shufei Lei3Susan T. L. Harrison4Spencer Diamond5Jillian F. Banfield6The Innovative Genomics Institute at the University of CaliforniaReasearch Office, Faculty of Health Sciences, University of Cape TownThe Innovative Genomics Institute at the University of CaliforniaThe Department of Earth and Planetary Science, University of CaliforniaThe Center for Bioprocess Engineering Research, University of Cape TownThe Innovative Genomics Institute at the University of CaliforniaThe Innovative Genomics Institute at the University of CaliforniaAbstract Metagenomic or metabarcoding data are often used to predict microbial interactions in complex communities, but these predictions are rarely explored experimentally. Here, we use an organism abundance correlation network to investigate factors that control community organization in mine tailings-derived laboratory microbial consortia grown under dozens of conditions. The network is overlaid with metagenomic information about functional capacities to generate testable hypotheses. We develop a metric to predict the importance of each node within its local network environments relative to correlated vitamin auxotrophs, and predict that a Variovorax species is a hub as an important source of thiamine. Quantification of thiamine during the growth of Variovorax in minimal media show high levels of thiamine production, up to 100 mg/L. A few of the correlated thiamine auxotrophs are predicted to produce pantothenate, which we show is required for growth of Variovorax, supporting that a subset of vitamin-dependent interactions are mutualistic. A Cryptococcus yeast produces the B-vitamin pantothenate, and co-culturing with Variovorax leads to a 90-130-fold fitness increase for both organisms. Our study demonstrates the predictive power of metagenome-informed, microbial consortia-based network analyses for identifying microbial interactions that underpin the structure and functioning of microbial communities.https://doi.org/10.1038/s41467-023-40360-4 |
| spellingShingle | Tomas Hessler Robert J. Huddy Rohan Sachdeva Shufei Lei Susan T. L. Harrison Spencer Diamond Jillian F. Banfield Vitamin interdependencies predicted by metagenomics-informed network analyses and validated in microbial community microcosms Nature Communications |
| title | Vitamin interdependencies predicted by metagenomics-informed network analyses and validated in microbial community microcosms |
| title_full | Vitamin interdependencies predicted by metagenomics-informed network analyses and validated in microbial community microcosms |
| title_fullStr | Vitamin interdependencies predicted by metagenomics-informed network analyses and validated in microbial community microcosms |
| title_full_unstemmed | Vitamin interdependencies predicted by metagenomics-informed network analyses and validated in microbial community microcosms |
| title_short | Vitamin interdependencies predicted by metagenomics-informed network analyses and validated in microbial community microcosms |
| title_sort | vitamin interdependencies predicted by metagenomics informed network analyses and validated in microbial community microcosms |
| url | https://doi.org/10.1038/s41467-023-40360-4 |
| work_keys_str_mv | AT tomashessler vitamininterdependenciespredictedbymetagenomicsinformednetworkanalysesandvalidatedinmicrobialcommunitymicrocosms AT robertjhuddy vitamininterdependenciespredictedbymetagenomicsinformednetworkanalysesandvalidatedinmicrobialcommunitymicrocosms AT rohansachdeva vitamininterdependenciespredictedbymetagenomicsinformednetworkanalysesandvalidatedinmicrobialcommunitymicrocosms AT shufeilei vitamininterdependenciespredictedbymetagenomicsinformednetworkanalysesandvalidatedinmicrobialcommunitymicrocosms AT susantlharrison vitamininterdependenciespredictedbymetagenomicsinformednetworkanalysesandvalidatedinmicrobialcommunitymicrocosms AT spencerdiamond vitamininterdependenciespredictedbymetagenomicsinformednetworkanalysesandvalidatedinmicrobialcommunitymicrocosms AT jillianfbanfield vitamininterdependenciespredictedbymetagenomicsinformednetworkanalysesandvalidatedinmicrobialcommunitymicrocosms |