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.
Highlights
The quest to manipulate microbiomes has intensified, but many microbial communities have proven to be recalcitrant to sustained change
We developed a model system involving three bacterial species, Pseudomonas koreensis, Flavobacterium johnsoniae, and Bacillus cereus, which interact under field and laboratory conditions, are amenable to genetic analysis, and represent three major phyla in microbiomes on plant roots and in the human gut
We propose that B. cereus protects F. johnsoniae by selectively reducing the levels of koreenceine A and C accumulated by P. koreensis
Summary
The quest to manipulate microbiomes has intensified, but many microbial communities have proven to be recalcitrant to sustained change. Powerful -omics approaches that profile community features such as genomes, metabolites, and transcripts have illuminated the richness of many communities [1] These global portraits of complex communities have been complemented by genetic and biochemical dissection of much simpler communities and, in particular, binary interactions of one bacterial species with one host, such as bacterial symbionts of legume roots [2] and squid light organs [3]. Key among the traits that demand more mechanistic studies are the components of community assembly and robustness, which is the ability to resist and recover from change [8, 9] Understanding these traits has particular value today, as many researchers aim to modify microbial communities to achieve outcomes to improve human health, environmental sustainability, and agricultural productivity. Few treatments have induced long-term changes due to intrinsic community robustness
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