Symbionts for pathogen defense in beewolves

Beewolves of the genera Philanthus, Trachypus, and Philanthinus (Hymenoptera, Crabronidae) are solitary digger wasps that engage in a highly specialized symbiotic association with high-GC gram-positive Actinobacteria (‘Candidatus Streptomyces philanthi’). The bacteria are cultivated in specialized antennal gland reservoirs of female wasps and secreted into the subterranean brood cells. The wasp larva later actively transfers the symbionts to its cocoon, where the streptomycetes provide protection against a broad range of opportunistic fungi and bacteria by producing at least nine different antibiotics (streptochlorin and eight piericidins). We detected ‘Ca. S. philanthi’ in about 40 different beewolf species, with the symbionts forming a well-defined monophyletic clade within the genus Streptomyces, suggesting a highly specific association between the wasps and ‘Ca. S. philanthi’ that probably originated in the late Cretaceous (at least 68 million years ago).

We are interested in the chemical and molecular interactions between the symbiotic partners of the beewolf-Streptomyces symbiosis as well as the genomic consequences of the symbiotic lifestyle for the bacteria. We are currently analyzing the bacterial compounds that are responsible for the protection of the beewolf offspring against pathogens and the substances that the beewolves provide for the growth of the bacteria in the antennal gland reservoirs. Furthermore, we are sequencing the whole genome of several different symbiont strains. The genome sequences will not only allow us to identify potential antibiotic genes, it will also shed light on the genomic consequences of the symbiotic lifestyle for the bacteria. Intracellular symbionts of insects have been shown to suffer dramatic genome reduction, rearrangements and shifts in base composition as compared to free-living relatives. The genome sequence of ‘Ca. Streptomyces philanthi’ will reveal the effects of an extracellular mutualistic lifestyle on genome architecture of a high-GC Gram-positive bacterium and thereby allow us to draw more general conclusions on the evolutionary and genomic consequences of insect-bacteria symbioses.

Martin Kaltenpoth, Tobias Engl, Mario Sandoval-Calderón, Chantal Selina Ingham

Selected publications:

Strohm, E., Herzner, G., Ruther, J., Kaltenpoth, M., Engl, T. (2019) Nitric oxide radicals are emitted by wasp eggs to kill mold fungi. eLife, doi; 10.7554/eLife.43718

Engl, T., Kroiss, J., Kai, M., Nechitaylo, T., Svatoš, A.,Kaltenpoth, M. (2018). Evolutionary stability of antibiotic protection in a defensive symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 115 (9)_: E2020-E2029.

Kaltenpoth, M. (2016) Symbiotic Streptomyces provide antifungal defense in solitary wasps. In: Hurst, C.J. (ed.) Advances in environmental microbiology: The mechanistic benefits of microbial symbionts. Springer, Heidelberg.

Kaltenpoth, M., Roeser-Mueller, K., Koehler, S., Peterson, A., Nechitaylo, T., Stubblefield, J.W., Herzner, G., Seger, J. & Strohm, E. (2014) Partner choice and fidelity stabilize co-evolution in a cretaceous-age defensive symbiosis. Proceedings of the National Academy of Sciences of the USA 111 (17): 6359-6364.

Nechitaylo, T.Y., Westermann, M. & Kaltenpoth, M. (2014) Cultivation reveals physiological diversity among defensive ‘Streptomyces philanthi’ symbionts of beewolf digger wasps (Hymenoptera, Crabronidae). BMC Microbiology 14: 202.

Koehler, S. & Kaltenpoth, M. (2013) Maternal and environmental effects on symbiont-mediated antimicrobial defense. Journal of Chemical Ecology 39 (7): 978-988 (invited contribution).

Koehler, S., Doubský, J. & Kaltenpoth, M. (2013) Dynamics of symbiont-mediated antibiotic production reveal efficient long-term protection for beewolf offspring. Frontiers in Zoology 10:3.

Kaltenpoth, M., Yildirim, E., Gürbüz, M. F., Herzner, G., Strohm, E. (2012) Refining the roots of the beewolf-Streptomyces symbiosis: Antennal symbionts in the rare genus Philanthinus (Hymenoptera, Crabronidae). Applied and Environmental Microbiology 78 (3): 822-827.

Kaltenpoth, M., Schmitt, T., Polidori, C., Koedam, D., Strohm, E. (2010) Symbiotic streptomycetes in antennal glands of the South American digger wasps genus Trachypus (Hymenoptera: Crabronidae). Physiological Entomology 35 (2): 196-200.

Kroiss, J., Kaltenpoth, M., Schneider, B., Schwinger, M.-G., Hertweck, C., Maddula, R.K., Strohm, E. & Svatoš, A. (2010) Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nature Chemical Biology 6: 261-263.

Kaltenpoth, M., Goettler, W., Koehler, S. & Strohm, E. (2010) Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission. Evolutionary Ecology 24 (2): 463-477.

Goettler, W., Kaltenpoth, M., Herzner, G. & Strohm, E. (2007) Morphology and ultrastructure of a bacteria cultivation organ: The antennal glands of female European beewolves, Philanthus triangulum (Hymenoptera, Crabronidae). Arthropod Structure and Development 36: 1-9.

Kaltenpoth, M., Göttler, W., Dale, C., Stubblefield, J.W., Herzner, G., Roeser-Mueller, K. & Strohm, E. (2006). 'Candidatus Streptomyces philanthi', an endosymbiotic streptomycete in the antennae of Philanthus digger wasps. International Journal of Systematic and Evolutionary Microbiology 56 (6): 1403-1411.

Kaltenpoth, M., Goettler, W., Herzner, G. & Strohm, E. (2005). Symbiotic bacteria protect wasp larvae from fungal infestation. Current Biology 15 (5): 475-479.