Article

A bacterial symbiont is converted from an inedible producer of beneficial molecules into food by a single mutation in the gacA gene

Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115.
Proceedings of the National Academy of Sciences (Impact Factor: 9.81). 07/2013; 110(36). DOI: 10.1073/pnas.1308199110
Source: PubMed

ABSTRACT Stable multipartite mutualistic associations require that all partners benefit. We show that a single mutational step is sufficient to turn a symbiotic bacterium from an inedible but host-beneficial secondary metabolite producer into a host food source. The bacteria's host is a "farmer" clone of the social amoeba Dictyostelium discoideum that carries and disperses bacteria during its spore stage. Associated with the farmer are two strains of Pseudomonas fluorescens, only one of which serves as a food source. The other strain produces diffusible small molecules: pyrrolnitrin, a known antifungal agent, and a chromene that potently enhances the farmer's spore production and depresses a nonfarmer's spore production. Genome sequence and phylogenetic analyses identify a derived point mutation in the food strain that generates a premature stop codon in a global activator (gacA), encoding the response regulator of a two-component regulatory system. Generation of a knockout mutant of this regulatory gene in the nonfood bacterial strain altered its secondary metabolite profile to match that of the food strain, and also, independently, converted it into a food source. These results suggest that a single mutation in an inedible ancestral strain that served a protective role converted it to a "domesticated" food source.

0 Followers
 · 
151 Views
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Background The social amoeba Dictyostelium discoideum interacts with bacteria in a variety of ways. It is a predator of bacteria, can be infected or harmed by bacteria, and can form symbiotic associations with bacteria. Some clones of D. discoideum function as primitive farmers because they carry bacteria through the normally sterile D. discoideum social stage, then release them after dispersal so the bacteria can proliferate and be harvested. Some farmer-associated bacteria produce small molecules that promote host farmer growth but inhibit the growth of non-farmer competitors. To test whether the farmers¿ tolerance is specific or extends to other growth inhibitory bacteria, we tested whether farmer and non-farmer amoebae are differentially affected by E. coli strains of varying pathogenicity. Because the numbers of each organism may influence the outcome of amoeba-bacteria interactions, we also examined the influence of amoeba and bacteria density on the ability of D. discoideum to grow and develop on distinct bacterial strains.ResultsA subset of E. coli strains did not support amoeba proliferation on rich medium, independent of whether the amoebae were farmers or non-farmers. However, amoebae could proliferate on these strains if amoebae numbers are high relative to bacteria numbers, but again there was no difference in this ability between farmer and non-farmer clones of D. discoideum.Conclusions Our results show that farmer and non-farmers did not differ in their abilities to consume novel strains of E. coli, suggesting that farmer resistance to their own carried bacteria does not extend to foreign bacteria. We see that increasing the numbers of bacteria or amoebae increases their respective likelihood of competitive victory over the other, thus showing Allee effects. We hypothesize that higher bacteria numbers may result in higher concentrations of a toxic product or in a reduction of resources critical for amoeba survival, producing an environment inhospitable to amoeba predators. Greater amoeba numbers may counter this growth inhibition, possibly through reducing bacterial numbers via increased predation rates, or by producing something that neutralizes a potentially toxic bacterial product.
    BMC Microbiology 12/2014; 14(1):328. DOI:10.1186/PREACCEPT-1930081937138331 · 2.98 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: ABSTRACT We report that establishment and maintenance of the Drosophila melanogaster microbiome depend on ingestion of bacteria. Frequent transfer of flies to sterile food prevented establishment of the microbiome in newly emerged flies and reduced the predominant members, Acetobacter and Lactobacillus spp., by 10- to 1,000-fold in older flies. Flies with a normal microbiome were less susceptible than germfree flies to infection by Serratia marcescens and Pseudomonas aeruginosa. Augmentation of the normal microbiome with higher populations of Lactobacillus plantarum, a Drosophila commensal and probiotic used in humans, further protected the fly from infection. Replenishment represents an unexplored strategy by which animals can sustain a gut microbial community. Moreover, the population behavior and health benefits of L. plantarum resemble features of certain probiotic bacteria administered to humans. As such, L. plantarum in the fly gut may serve as a simple model for dissecting the population dynamics and mode of action of probiotics in animal hosts. IMPORTANCE Previous studies have defined the composition of the Drosophila melanogaster microbiome in laboratory and wild-caught flies. Our study advances current knowledge in this field by demonstrating that Drosophila must consume bacteria to establish and maintain its microbiome. This finding suggests that the dominant Drosophila symbionts remain associated with their host because of repeated reintroduction rather than internal growth. Furthermore, our study shows that one member of the microbiome, Lactobacillus plantarum, protects the fly from intestinal pathogens. These results suggest that, although not always present, the microbiota can promote salubrious effects for the host. In sum, our work provides a previously unexplored mechanism of microbiome maintenance and an in vivo model system for investigating the mechanisms of action of probiotic bacteria.
    mBio 10/2013; 4(6). DOI:10.1128/mBio.00860-13 · 6.88 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Multitrophic level microbial loop interactions mediated by protist predators, bacteria and viruses drive eco- and agro-biotechnological processes such as bioremediation, wastewater treatment, plant growth promotion and ecosystem functioning. To what extent these microbial interactions are context-dependent in performing biotechnological and ecosystem processes remains largely unstudied. Theory-driven research may advance the understanding of eco-evolutionary processes underlying the patterns and functioning of microbial interactions for successful development of microbe-based biotechnologies for real world applications. This could also be a great avenue to test the validity or limitations of ecology theory for managing diverse microbial resources in an era of altering microbial niches, multitrophic interactions and microbial diversity loss caused by climate and land use changes.
    Trends in Biotechnology 10/2014; 32(10):529–537. DOI:10.1016/j.tibtech.2014.08.002 · 10.04 Impact Factor