MCA: The role of symbiont toxins in a defensive mutualism

Symbioses between animals and microbes are ubiquitous in nature and can strongly influence the ability of animals to use resources and cope with different environmental stressors and disease. An emerging and exciting theme in symbiosis is the ability of microbes, particularly bacteria, to protect their hosts against natural enemies. Such defensive associations are highly pertinent to agriculture and human health, as they can influence, in negative and positive ways, the effectiveness of measures targeted at diverse insect pests and insect-vectored pathogens.

Although records of such defensive associations have rapidly accrued, knowledge of how these bacteria defend their hosts is lagging. Studying such interactions is difficult because it is usually not possible to grow and manipulate the bacterial partner independently of the insect. This project capitalizes on the powerful research tools available with the fruit fly (Drosophila melanogaster) model system to understand the role of toxins produced by an inherited bacterium (Spiroplasma) that protects flies against parasitic wasps.

This project will also leverage exciting natural variation in the ‘three-way’ bacterium-fly-wasp interaction to uncover how certain wasps are able to avoid damage caused by the bacterium. These studies will help identify the general principles governing symbiont-mediated defense in nature. This project will broaden the participation of underrepresented groups in science and enhance scientific literacy, through research experiences for undergraduate and graduate students, as well as in-class and outreach activities.

The taxonomic diversity of hosts, symbionts, and natural enemies recorded in defensive associations is broad and rapidly growing, but understanding of the defensive mechanisms themselves is mostly restricted to a few associations involving members of a single bacterial group (Proteobacteria). Research progress has been hampered by the paucity of genetic and laboratory resources available for non-model hosts, symbionts, and natural enemies, precluding identification of general principles governing symbiont-mediated defense.

This project investigates a system involving an influential bacterial lineage (genus Spiroplasma: Class Mollicutes) that is not only highly divergent but is also distinct from the best studied defensive symbionts. Several lines of evidence suggest that the mechanism by which Spiroplasma prevents the successful development of wasps that parasitize Drosophila, involves a Spiroplasma-encoded toxin.

However, whether the toxin is necessary and sufficient to inhibit wasps has not been demonstrated; a task that is hampered by the inability to successfully transform Spiroplasma. This project will use bacteria-free transgenic Drosophila, to carefully examine whether the Spiroplasma-encoded toxin can disable wasps that parasitize Drosophila larvae. Complementary experiments will investigate the mechanism(s) by which certain wasp species are able to avoid damage by Spiroplasma.

Therefore, this project will yield novel insights into the mechanistic underpinnings of a tripartite coevolutionary arms race that is emerging as a model system.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.