Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring

Kroiß, Johannes; Kaltenpoth, Martin; Schneider, Bernd; Schwinger, Maria-Gabriele; Hertweck, Christian; Maddula, Ravi Kumar; Strohm, Erhard; Svatoš, Aleš

doi:10.1038/nchembio.331

Cited by 343 publications

(317 citation statements)

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“…Chemically uncharacterized supernatants collected from different non-food bacteria carried by other D. discoideum clones also help their farmer clone and harm non-carrier clones (37). Taken together, these observations provide a strong argument for coevolution of both the farmer and symbionts; they also establish that the symbiosis is not just a food and farmer symbiosis, but rather displays some of the multipartite qualities of other farming symbioses, such as the fungus-farming ants and bark beetles with their crop fungi providing the food and the bacterial symbionts providing chemical defenses against fungal pathogens (5,(7)(8)(9). What distinguishes this farming symbiosis is the close relatedness of PfB and PfA-the bacterial food source and the small-molecule producer (although this close relatedness does not hold for bacterial symbionts of other Dictyostelium farmers).…”

Section: A Single Mutation Determines Both Chemical Profile Changes Andmentioning

confidence: 81%

“…A fascinating set of structurally diverse molecules that defend the host, initiate host developmental changes, and carry out other important functions have been shaped by their evolutionary history (1)(2)(3)(4)(5)(6)(7)(8)(9)(10). Recently, Brock et al (11) described an association between the social amoeba Dictyostelium discoideum and a variety of Gram-negative bacteria, some of which it carries to initiate new food populations.…”

mentioning

confidence: 99%

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

Stallforth

Brock

Cantley

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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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 twocomponent 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.symbiosis | GacA-GacS two-component system | differential metabolomics S mall molecules regulate mutually beneficial associations between bacterial symbionts and their eukaryotic hosts. A fascinating set of structurally diverse molecules that defend the host, initiate host developmental changes, and carry out other important functions have been shaped by their evolutionary history (1-10). Recently, Brock et al. (11) described an association between the social amoeba Dictyostelium discoideum and a variety of Gram-negative bacteria, some of which it carries to initiate new food populations.D. discoideum is a popular model for studying multicellularity, chemical signaling, general eukaryotic cellular mechanisms, and social phenomena (12-15). The protist is typically found in soil, where it preys on bacteria; in nutrient-rich environments it lives as single-celled organisms that reproduce by binary fission. Upon starvation, cAMP-mediated aggregation occurs, leading to the formation of a multicellular pseudoplasmodium containing up to 10 5 individual cells. Eventually, the aggregate develops into a fruiting body in which some 20% of the cells differentiate into a dead stalk that supports a spherical structure known as the sorus; the latter contains 80% of the cells that turn into spores.Previous work by Brock et al. (11) showed that about one-third of wild-collected clones of D. discoideum engage in stable associations with bacteria throughout the sporulation and dispersal process. These clones are called "primitive farmers" because they carry, seed, and prudently harvest their bacterial food.Schultz and Brady (16) characterized agriculture as a specialized form of symbiosis known in only four animal groups: humans,...

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Section: A Single Mutation Determines Both Chemical Profile Changes Andmentioning

confidence: 81%

mentioning

confidence: 99%

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

Stallforth

Brock

Cantley

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Considering the weight of the A. echinatior workers used for the MALDI imaging (∼6 mg), several nanograms of valinomycin (3) and in some patches, several tenths of nanograms are likely to be sufficient to fight against susceptible organisms. Until now, it has only been possible to directly detect antibiotics of microbial symbionts from insects on the cocoon of beewolf larvae (45). The presence of valinomycin (3) on the ants' bodies suggests that it may play an important role in protecting individual workers, probably not only against microbial pathogens but also against parasites (e.g., mites) (1,42).…”

Section: Discussionmentioning

confidence: 99%

Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants

Schoenian

Spiteller

Ghaste

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

169

187

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Leaf-cutting ants cultivate the fungus Leucoagaricus gongylophorus, which serves as a major food source. This symbiosis is threatened by microbial pathogens that can severely infect L. gongylophorus. Microbial symbionts of leaf-cutting ants, mainly Pseudonocardia and Streptomyces, support the ants in defending their fungus gardens against infections by supplying antimicrobial and antifungal compounds. The ecological role of microorganisms in the nests of leaf-cutting ants can only be addressed in detail if their secondary metabolites are known. Here, we use an approach for the rapid identification of established bioactive compounds from microorganisms in ecological contexts by combining phylogenetic data, database searches, and liquid chromatography electrospray ionisation high resolution mass spectrometry (LC-ESI-HR-MS) screening. Antimycins A 1 -A 4 , valinomycins, and actinomycins were identified in this manner from Streptomyces symbionts of leaf-cutting ants. Matrix-assisted laser desorption ionization (MALDI) imaging revealed the distribution of valinomycin directly on the integument of Acromyrmex echinatior workers. Valinomycins and actinomycins were also directly identified in samples from the waste of A. echinatior and A. niger leaf-cutting ants, suggesting that the compounds exert their antimicrobial and antifungal potential in the nests of leaf-cutting ants. Strong synergistic effects of the secondary metabolites produced by ant-associated Streptomyces were observed in the agar diffusion assay against Escovopsis weberi. Actinomycins strongly inhibit soil bacteria as well as other Streptomyces and Pseudonocardia symbionts. The antifungal antimycins are not only active against pathogenic fungi but also the garden fungus L. gongylophorus itself. In conclusion, secondary metabolites of microbial symbionts of leaf-cutting ants contribute to shaping the microbial communities within the nests of leaf-cutting ants.

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“…Numerous bacteriocins produced by the intestinal microbiota are active against potential pathogens such as Listeria, Salmonella and Clostridium species (Dabard et al, 2001;Gong et al, 2010;Rea et al, 2010). Cuticular Streptomycetes bacteria are protecting the offspring of digger wasps from fungal pathogens by producing a complex cocktail of antibiotics (Kroiss et al, 2010). The role of individual members of a highly diverse bacterial community associated with a host remains largely unclear.…”

Section: Introductionmentioning

confidence: 99%

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

et al. 2014

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Epithelial surfaces of most animals are colonized by diverse microbial communities. Although it is generally agreed that commensal bacteria can serve beneficial functions, the processes involved are poorly understood. Here we report that in the basal metazoan Hydra, ectodermal epithelial cells are covered with a multilayered glycocalyx that provides a habitat for a distinctive microbial community. Removing this epithelial microbiota results in lethal infection by the filamentous fungus Fusarium sp. Restoring the complex microbiota in gnotobiotic polyps prevents pathogen infection. Although mono-associations with distinct members of the microbiota fail to provide full protection, additive and synergistic interactions of commensal bacteria are contributing to full fungal resistance. Our results highlight the importance of resident microbiota diversity as a protective factor against pathogen infections. Besides revealing insights into the in vivo function of commensal microbes in Hydra, our findings indicate that interactions among commensal bacteria are essential to inhibit pathogen infection.

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Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring

Cited by 343 publications

References 19 publications

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

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

Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

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