Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring

Journal name:
Nature Chemical Biology
Volume:
6,
Pages:
261–263
Year published:
DOI:
doi:10.1038/nchembio.331
Received
Accepted
Published online

Beewolf digger wasps cultivate specific symbiotic bacteria (Streptomyces spp.) that are incorporated into the larval cocoon for protection against pathogens. We identified the molecular basis of this protective symbiosis in the natural context and demonstrate that the bacteria produce a 'cocktail' of nine antibiotic substances. The complementary action of all symbiont-produced antibiotics confers a potent antimicrobial defense for the wasp larvae that parallels the 'combination prophylaxis' known from human medicine.

At a glance

Figures

  1. Wasp symbionts from female antennae produce an antibiotic cocktail on the larval cocoon.
    Figure 1: Wasp symbionts from female antennae produce an antibiotic cocktail on the larval cocoon.

    (a) Female European beewolf secreting symbiotic streptomycetes (white areas) from antennal glands onto the brood cell ceiling (brood cell covered with a glass plate in an observation cage). (b) Fluorescence in situ hybridization (FISH) micrograph of beewolf symbionts in the antennal gland secretion using the specific Cy3-labeled probe SPT177 (in pseudocolors)7, 8. (c) Antibiotic substances isolated from beewolf cocoons: streptochlorin (left) and eight piericidin derivatives (right). (d) Mass spectrometric imaging (LDI-TOF/MS) of the three most abundant antibiotic substances on a beewolf cocoon. Ion intensity maps of piericidin A1 (m/z 454 ± 0.5 [M+K]+) (upper left), piericidin B1 (m/z 468 ± 0.5 [M+K]+) (upper right) and streptochlorin (m/z 219 ± 0.5 [M+H]+) (lower left). Intensities of ions in the imaged spots are color coded using a heat map; black corresponds to 0 and red corresponds to 255 counts. Lower right: photograph of the cocoon used for LDI-TOF/MS imaging mounted on a MALDI target plate (scale bar, 5 mm).

  2. Biological activity of antibiotic substances produced by beewolf symbionts.
    Figure 2: Biological activity of antibiotic substances produced by beewolf symbionts.

    (a) Representative picture of an agar-diffusion assay with single-cocoon equivalents of crude beewolf cocoon extract (i) and four individual antibiotic substances (ii, streptochlorin; iii, piericidin A1; iv, piericidin B1; v, glucopiericidin A) as well as a positive control (vi, nystatin) against Penicillium avellaneum. (b) Inhibition of ten strains of ubiquitous and entomopathogenic fungi and bacteria by antibiotic substances produced by beewolf symbionts (red, maximum inhibition zone; orange, 76–99%; yellow, 51–75%; green, 26–50%; gray, 1–25% of maximum inhibition zone). (c) Dose-response curve for ten fungal and bacterial pathogens for piericidin A1 (Aspergillus fumigatus, black circle; Aspergillus flavus, purple rhombus; Penicillium notatum, pink circle; Penicillium avellaneum, orange inverted triangle; Sporobolomyces salmonicolor, light green inverted triangle; Fusarium oxysporum, yellow square; Metarhizium anisopliae, red triangle; Beauveria bassiana, dark blue triangle; Bacillus subtilis, blue square; Paenibacillus larvae, green rhombus). Bottom of c: amount of piericidin A1 present on single cocoons (the bold line represents the median, the box comprises the interquartile range and the bars indicate minimum and maximum values).

Compounds

9 compounds View all compounds
  1. Streptochlorin
    Compound 1 Streptochlorin
  2. Piericidin A1
    Compound 2 Piericidin A1
  3. Piericidin B1
    Compound 3 Piericidin B1
  4. Glucopiericidin A
    Compound 4 Glucopiericidin A
  5. Piericidin A5
    Compound 5 Piericidin A5
  6. Piericidin C1
    Compound 6 Piericidin C1
  7. 9'-Demethyl-piericidin A1
    Compound 7 9'-Demethyl-piericidin A1
  8. Piericidin B5
    Compound 8 Piericidin B5
  9. Piericidin IT-143-B
    Compound 9 Piericidin IT-143-B

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Author information

Affiliations

  1. Research Group Mass Spectrometry, Max Planck Institute for Chemical Ecology, Jena, Germany.

    • Johannes Kroiss,
    • Ravi Kumar Maddula &
    • Aleš Svatoš
  2. Department of Zoology, University of Regensburg, Regensburg, Germany.

    • Martin Kaltenpoth &
    • Erhard Strohm
  3. Research Group Biosynthesis/NMR, Max Planck Institute for Chemical Ecology, Jena, Germany.

    • Bernd Schneider
  4. Leibniz Institute for Natural Product Research and Infection Biology (Hans Knöll Institute), Jena, Germany.

    • Maria-Gabriele Schwinger &
    • Christian Hertweck
  5. Present address: Research Group Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany.

    • Johannes Kroiss &
    • Martin Kaltenpoth

Contributions

J.K., A.S. and M.K. conceived of the study. J.K. and A.S. isolated, identified and quantified the antibiotic substances and performed the imaging mass spectrometry. J.K., A.S., M.K. and E.S. wrote the manuscript. B.S. carried out the NMR experiments. M.-G.S. and C.H. performed the biological activity experiments. R.K.M. conducted the MS-MS experiments. M.K. and E.S. carried out the GC-MS experiments.

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The authors declare no competing financial interests.

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