Symbiotic bacteria: from hitchhikers to bodyguards
As a plant pathogen, hitching a ride on an herbivorous insect to get to your favorite destination can make a lot of sense. Protecting the driver to fix a long-term deal is probably even smarter. In our recent paper, we describe how a bacterium with plant pathogenic ancestry has become a defensive symbiont of a beetle thanks to the production of a range of bioactive compounds.
The bacterium Burkholderia gladioli can live in various environments, and is best known for causing disease in a number of plants. To our surprise, we found the same bacteria inside a pair of glands in the reproductive system of a group of widespread herbivorous beetles, the Lagriinae. We tracked the bacteria throughout the life cycle of the beetle and confirmed that they are transmitted from mother to offspring, in a secretion applied during egg-laying. The bacteria then colonize three invaginations forming in the back of the embryo. As far as we know, this kind of symbiont-bearing structures haven’t been described in the larvae of any other insect. Since the bacteria seem to have such a tight and consistent association with the beetles, we very much expected some kind of benefit to the insect for carrying them. To test this, we generated symbiont-free beetles and looked for possible effects. Fine-tuning this method took a while, and finding many of the precious eggs overgrown by a lawn of mold was at first more disappointing than anything else. Excitement came later, when we realized this seemed to happen much more frequently in the symbiont-free eggs than in the “normal” symbiotic ones. We set up a more rigorous experiment to test for symbiont-provided antifungal protection, and indeed, the bacteria turned out to be excellent bodyguards.
Symbiotic bacteria in high density inside the glands of Lagria villosa beetles. You can see the symbionts in yellow and the insect cell nuclei in blue.
The next question in line was how the symbionts manage to protect. Burkholderia bacteria are known to produce a range of bioactive secondary metabolites, and to our luck, there was a group of experts in exactly this topic just down the road, at the Leibniz Institute for Natural Product Research and Infection Biology. We teamed up with researchers from Christian Hertweck’s group, and they discovered several interesting compounds from the B. gladioli symbionts that indeed inhibited the fungi we had isolated, as well as a range of other bacteria and fungi. Two of the compounds they found were new. In one of them, part of the chemical structure –an isothiocyanate moiety- resembles a kind of plant defensive molecule (mustard oils) rather than compounds usually expected from bacteria. The new molecule was named sinapigladioside, given its connection to mustard or “sinapis” in latin.
We kept in the back of our minds that B. gladioli are often plant pathogenic. This triggered a late chat with Martin after one of our journal clubs. We had discussed Enric Frago, Marcel Dicke and Charles Godfray´s review on insect-plant-microbe interactions, and Martin was excited to think that a multipartite interaction involving the plant could be especially relevant in the Lagria system. Soybean was our plant of choice, since one of the beetle species occurs in large numbers in Brazilian soybean plantations. We found out that the adults could in fact transfer Burkholderia bacteria to the plant tissues and later Paul Gaube, an M.Sc. student in our group, showed that the bacterial symbionts can systemically infect the plants and cause a decline in seed numbers. It became clear that they can still interact with a plant host and affect it negatively despite the mutualistic association with the beetles.
From the beetle's perspective.
Plants as a common environment and the ability of B. gladioli to produce bioactive compounds was likely central to the evolution of this symbiosis, and gave rise to a seemingly key innovation for vulnerable offspring protection in the beetles. This might also be true for many other arthropods that can transmit associated microbes via the egg, especially those in which this stage is particularly threatened. In these or similar cases, microbial symbionts might be a treasure trove of antibiotics with promising applications, and they also provide exciting insights into the tricks that animals and microbes play to team up and fight their enemies.
If you want to check out more details on this particular trick, you can find the paper in Nature Communications here: http://go.nature.com/2qenO8x