Deciphering microbial interactions in synthetic human gut microbiome communities
Abstract The ecological forces that govern the assembly and stability of the human gut microbiota remain unresolved. We developed a generalizable model‐guided framework to predict higher‐dimensional consortia from time‐resolved measurements of lower‐order assemblages. This method was employed to dec...
Saved in:
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Springer Nature
2018-06-01
|
| Series: | Molecular Systems Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.15252/msb.20178157 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849738682675757056 |
|---|---|
| author | Ophelia S Venturelli Alex V Carr Garth Fisher Ryan H Hsu Rebecca Lau Benjamin P Bowen Susan Hromada Trent Northen Adam P Arkin |
| author_facet | Ophelia S Venturelli Alex V Carr Garth Fisher Ryan H Hsu Rebecca Lau Benjamin P Bowen Susan Hromada Trent Northen Adam P Arkin |
| author_sort | Ophelia S Venturelli |
| collection | DOAJ |
| description | Abstract The ecological forces that govern the assembly and stability of the human gut microbiota remain unresolved. We developed a generalizable model‐guided framework to predict higher‐dimensional consortia from time‐resolved measurements of lower‐order assemblages. This method was employed to decipher microbial interactions in a diverse human gut microbiome synthetic community. We show that pairwise interactions are major drivers of multi‐species community dynamics, as opposed to higher‐order interactions. The inferred ecological network exhibits a high proportion of negative and frequent positive interactions. Ecological drivers and responsive recipient species were discovered in the network. Our model demonstrated that a prevalent positive and negative interaction topology enables robust coexistence by implementing a negative feedback loop that balances disparities in monospecies fitness levels. We show that negative interactions could generate history‐dependent responses of initial species proportions that frequently do not originate from bistability. Measurements of extracellular metabolites illuminated the metabolic capabilities of monospecies and potential molecular basis of microbial interactions. In sum, these methods defined the ecological roles of major human‐associated intestinal species and illuminated design principles of microbial communities. |
| format | Article |
| id | doaj-art-fabdf0a218ed497ea221a1d5902aab2f |
| institution | DOAJ |
| issn | 1744-4292 |
| language | English |
| publishDate | 2018-06-01 |
| publisher | Springer Nature |
| record_format | Article |
| series | Molecular Systems Biology |
| spelling | doaj-art-fabdf0a218ed497ea221a1d5902aab2f2025-08-20T03:06:29ZengSpringer NatureMolecular Systems Biology1744-42922018-06-0114611910.15252/msb.20178157Deciphering microbial interactions in synthetic human gut microbiome communitiesOphelia S Venturelli0Alex V Carr1Garth Fisher2Ryan H Hsu3Rebecca Lau4Benjamin P Bowen5Susan Hromada6Trent Northen7Adam P Arkin8Department of Biochemistry, University of Wisconsin‐MadisonEnvironmental Genomics and Systems Biology, Lawrence Berkeley National LaboratoryEnvironmental Genomics and Systems Biology, Lawrence Berkeley National LaboratoryCalifornia Institute for Quantitative Biosciences, University of California BerkeleyEnvironmental Genomics and Systems Biology, Lawrence Berkeley National LaboratoryEnvironmental Genomics and Systems Biology, Lawrence Berkeley National LaboratoryDepartment of Biochemistry, University of Wisconsin‐MadisonEnvironmental Genomics and Systems Biology, Lawrence Berkeley National LaboratoryEnvironmental Genomics and Systems Biology, Lawrence Berkeley National LaboratoryAbstract The ecological forces that govern the assembly and stability of the human gut microbiota remain unresolved. We developed a generalizable model‐guided framework to predict higher‐dimensional consortia from time‐resolved measurements of lower‐order assemblages. This method was employed to decipher microbial interactions in a diverse human gut microbiome synthetic community. We show that pairwise interactions are major drivers of multi‐species community dynamics, as opposed to higher‐order interactions. The inferred ecological network exhibits a high proportion of negative and frequent positive interactions. Ecological drivers and responsive recipient species were discovered in the network. Our model demonstrated that a prevalent positive and negative interaction topology enables robust coexistence by implementing a negative feedback loop that balances disparities in monospecies fitness levels. We show that negative interactions could generate history‐dependent responses of initial species proportions that frequently do not originate from bistability. Measurements of extracellular metabolites illuminated the metabolic capabilities of monospecies and potential molecular basis of microbial interactions. In sum, these methods defined the ecological roles of major human‐associated intestinal species and illuminated design principles of microbial communities.https://doi.org/10.15252/msb.20178157ecologyhuman gut microbiomemathematical modelingmicrobial communitymicrobial interaction |
| spellingShingle | Ophelia S Venturelli Alex V Carr Garth Fisher Ryan H Hsu Rebecca Lau Benjamin P Bowen Susan Hromada Trent Northen Adam P Arkin Deciphering microbial interactions in synthetic human gut microbiome communities Molecular Systems Biology ecology human gut microbiome mathematical modeling microbial community microbial interaction |
| title | Deciphering microbial interactions in synthetic human gut microbiome communities |
| title_full | Deciphering microbial interactions in synthetic human gut microbiome communities |
| title_fullStr | Deciphering microbial interactions in synthetic human gut microbiome communities |
| title_full_unstemmed | Deciphering microbial interactions in synthetic human gut microbiome communities |
| title_short | Deciphering microbial interactions in synthetic human gut microbiome communities |
| title_sort | deciphering microbial interactions in synthetic human gut microbiome communities |
| topic | ecology human gut microbiome mathematical modeling microbial community microbial interaction |
| url | https://doi.org/10.15252/msb.20178157 |
| work_keys_str_mv | AT opheliasventurelli decipheringmicrobialinteractionsinsynthetichumangutmicrobiomecommunities AT alexvcarr decipheringmicrobialinteractionsinsynthetichumangutmicrobiomecommunities AT garthfisher decipheringmicrobialinteractionsinsynthetichumangutmicrobiomecommunities AT ryanhhsu decipheringmicrobialinteractionsinsynthetichumangutmicrobiomecommunities AT rebeccalau decipheringmicrobialinteractionsinsynthetichumangutmicrobiomecommunities AT benjaminpbowen decipheringmicrobialinteractionsinsynthetichumangutmicrobiomecommunities AT susanhromada decipheringmicrobialinteractionsinsynthetichumangutmicrobiomecommunities AT trentnorthen decipheringmicrobialinteractionsinsynthetichumangutmicrobiomecommunities AT adamparkin decipheringmicrobialinteractionsinsynthetichumangutmicrobiomecommunities |