Introducing THOR, a Model Microbiome for Genetic Dissection of Community Behavior
ABSTRACT The quest to manipulate microbiomes has intensified, but many microbial communities have proven to be recalcitrant to sustained change. Developing model communities amenable to genetic dissection will underpin successful strategies for shaping microbiomes by advancing an understanding of co...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2019-04-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.02846-18 |
| _version_ | 1818346731860918272 |
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| author | Gabriel L. Lozano Juan I. Bravo Manuel F. Garavito Diago Hyun Bong Park Amanda Hurley S. Brook Peterson Eric V. Stabb Jason M. Crawford Nichole A. Broderick Jo Handelsman |
| author_facet | Gabriel L. Lozano Juan I. Bravo Manuel F. Garavito Diago Hyun Bong Park Amanda Hurley S. Brook Peterson Eric V. Stabb Jason M. Crawford Nichole A. Broderick Jo Handelsman |
| author_sort | Gabriel L. Lozano |
| collection | DOAJ |
| description | ABSTRACT The quest to manipulate microbiomes has intensified, but many microbial communities have proven to be recalcitrant to sustained change. Developing model communities amenable to genetic dissection will underpin successful strategies for shaping microbiomes by advancing an understanding of community interactions. We developed a model community with representatives from three dominant rhizosphere taxa, the Firmicutes, Proteobacteria, and Bacteroidetes. We chose Bacillus cereus as a model rhizosphere firmicute and characterized 20 other candidates, including “hitchhikers” that coisolated with B. cereus from the rhizosphere. Pairwise analysis produced a hierarchical interstrain-competition network. We chose two hitchhikers, Pseudomonas koreensis from the top tier of the competition network and Flavobacterium johnsoniae from the bottom of the network, to represent the Proteobacteria and Bacteroidetes, respectively. The model community has several emergent properties, induction of dendritic expansion of B. cereus colonies by either of the other members, and production of more robust biofilms by the three members together than individually. Moreover, P. koreensis produces a novel family of alkaloid antibiotics that inhibit growth of F. johnsoniae, and production is inhibited by B. cereus. We designate this community THOR, because the members are the hitchhikers of the rhizosphere. The genetic, genomic, and biochemical tools available for dissection of THOR provide the means to achieve a new level of understanding of microbial community behavior. IMPORTANCE The manipulation and engineering of microbiomes could lead to improved human health, environmental sustainability, and agricultural productivity. However, microbiomes have proven difficult to alter in predictable ways, and their emergent properties are poorly understood. The history of biology has demonstrated the power of model systems to understand complex problems such as gene expression or development. Therefore, a defined and genetically tractable model community would be useful to dissect microbiome assembly, maintenance, and processes. We have developed a tractable model rhizosphere microbiome, designated THOR, containing Pseudomonas koreensis, Flavobacterium johnsoniae, and Bacillus cereus, which represent three dominant phyla in the rhizosphere, as well as in soil and the mammalian gut. The model community demonstrates emergent properties, and the members are amenable to genetic dissection. We propose that THOR will be a useful model for investigations of community-level interactions. |
| first_indexed | 2024-12-13T17:22:56Z |
| format | Article |
| id | doaj.art-ebbf26fcf5c649b5b947227fd73e51c2 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-13T17:22:56Z |
| publishDate | 2019-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-ebbf26fcf5c649b5b947227fd73e51c22022-12-21T23:37:15ZengAmerican Society for MicrobiologymBio2150-75112019-04-0110210.1128/mBio.02846-18Introducing THOR, a Model Microbiome for Genetic Dissection of Community BehaviorGabriel L. Lozano0Juan I. Bravo1Manuel F. Garavito Diago2Hyun Bong Park3Amanda Hurley4S. Brook Peterson5Eric V. Stabb6Jason M. Crawford7Nichole A. Broderick8Jo Handelsman9Wisconsin Institute for Discovery and Department of Plant Pathology, University of Wisconsin-Madison, Madison, Wisconsin, USAWisconsin Institute for Discovery and Department of Plant Pathology, University of Wisconsin-Madison, Madison, Wisconsin, USAWisconsin Institute for Discovery and Department of Plant Pathology, University of Wisconsin-Madison, Madison, Wisconsin, USADepartment of Chemistry, Yale University, New Haven, Connecticut, USAWisconsin Institute for Discovery and Department of Plant Pathology, University of Wisconsin-Madison, Madison, Wisconsin, USADepartment of Microbiology, University of Washington, Seattle, Washington, USADepartment of Microbiology, University of Georgia, Athens, Georgia, USADepartment of Chemistry, Yale University, New Haven, Connecticut, USADepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USAWisconsin Institute for Discovery and Department of Plant Pathology, University of Wisconsin-Madison, Madison, Wisconsin, USAABSTRACT The quest to manipulate microbiomes has intensified, but many microbial communities have proven to be recalcitrant to sustained change. Developing model communities amenable to genetic dissection will underpin successful strategies for shaping microbiomes by advancing an understanding of community interactions. We developed a model community with representatives from three dominant rhizosphere taxa, the Firmicutes, Proteobacteria, and Bacteroidetes. We chose Bacillus cereus as a model rhizosphere firmicute and characterized 20 other candidates, including “hitchhikers” that coisolated with B. cereus from the rhizosphere. Pairwise analysis produced a hierarchical interstrain-competition network. We chose two hitchhikers, Pseudomonas koreensis from the top tier of the competition network and Flavobacterium johnsoniae from the bottom of the network, to represent the Proteobacteria and Bacteroidetes, respectively. The model community has several emergent properties, induction of dendritic expansion of B. cereus colonies by either of the other members, and production of more robust biofilms by the three members together than individually. Moreover, P. koreensis produces a novel family of alkaloid antibiotics that inhibit growth of F. johnsoniae, and production is inhibited by B. cereus. We designate this community THOR, because the members are the hitchhikers of the rhizosphere. The genetic, genomic, and biochemical tools available for dissection of THOR provide the means to achieve a new level of understanding of microbial community behavior. IMPORTANCE The manipulation and engineering of microbiomes could lead to improved human health, environmental sustainability, and agricultural productivity. However, microbiomes have proven difficult to alter in predictable ways, and their emergent properties are poorly understood. The history of biology has demonstrated the power of model systems to understand complex problems such as gene expression or development. Therefore, a defined and genetically tractable model community would be useful to dissect microbiome assembly, maintenance, and processes. We have developed a tractable model rhizosphere microbiome, designated THOR, containing Pseudomonas koreensis, Flavobacterium johnsoniae, and Bacillus cereus, which represent three dominant phyla in the rhizosphere, as well as in soil and the mammalian gut. The model community demonstrates emergent properties, and the members are amenable to genetic dissection. We propose that THOR will be a useful model for investigations of community-level interactions.https://journals.asm.org/doi/10.1128/mBio.02846-18Bacillus cereusFlavobacterium johnsoniaePseudomonas koreensisbiofilmcolony expansionemergent properties |
| spellingShingle | Gabriel L. Lozano Juan I. Bravo Manuel F. Garavito Diago Hyun Bong Park Amanda Hurley S. Brook Peterson Eric V. Stabb Jason M. Crawford Nichole A. Broderick Jo Handelsman Introducing THOR, a Model Microbiome for Genetic Dissection of Community Behavior mBio Bacillus cereus Flavobacterium johnsoniae Pseudomonas koreensis biofilm colony expansion emergent properties |
| title | Introducing THOR, a Model Microbiome for Genetic Dissection of Community Behavior |
| title_full | Introducing THOR, a Model Microbiome for Genetic Dissection of Community Behavior |
| title_fullStr | Introducing THOR, a Model Microbiome for Genetic Dissection of Community Behavior |
| title_full_unstemmed | Introducing THOR, a Model Microbiome for Genetic Dissection of Community Behavior |
| title_short | Introducing THOR, a Model Microbiome for Genetic Dissection of Community Behavior |
| title_sort | introducing thor a model microbiome for genetic dissection of community behavior |
| topic | Bacillus cereus Flavobacterium johnsoniae Pseudomonas koreensis biofilm colony expansion emergent properties |
| url | https://journals.asm.org/doi/10.1128/mBio.02846-18 |
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