Biology in 3D: our growing appreciation of
tripartite symbioses in nature
In recent years, biologists have had a growing appreciation for symbiosis. This comes from increased recognition of the importance of commonly known forms of symbiosis (e.g., mycorrhizas, legume-rhizobia), but also the discovery of many new symbioses in places we never thought to look before. Advances in microscopy, isotopic labeling and DNA sequencing have facilitated many of these discoveries, but most important has been the curiosity of scientists willing to look in new places. While mycologists have been at the forefront of symbiosis research, the focus has traditionally been on two way plant-fungal or animal-fungal interactions. However, recent research has unearthed evidence that threeway (tripartite) or even multipartite symbioses may in fact be the norm.
Perhaps the most commonly known tripartite symbiosis in the mycological world is that between trees, mycorrhizal fungi and non-photosynthetic plants. In this case the nonphotosynthetic plant parasitizes the fungus and use it like a straw to draw sugars from the tree. However, in recent years we’ve also learned about ectomycorrhizal fungi that parasitize nematodes as a source of nitrogen for their host trees, ectomycorrhizal fungi that may cultivate nitrogen-fixing bacteria, and an intricate four-way interaction between leaf cutter ants that cultivate fungal gardens and actinobacteria carried on the ants’ bodies that produce antibiotics to ward off other fungal parasites that might attack these gardens.
However, two tripartite symbiotic interactions were recently described that caught my attention and point towards an underlying complexity in the natural world that is at times hard to fathom. One of the most interesting things about these particular examples is that both involve endosymbionts (i.e., internal symbionts) living inside fungal hyphae.
The first example involves a tropical panic grass (Dichanthelium lanuginosum) that is able to grow under extremely high temperatures, such as those found at the shores of thermal hot springs at Yellowstone National Park. Earlier work showed that the presence of a fungal endosymbiont (Curvularia protuberata) was necessary for the plants to obtain this high-temperature phenotype. In the laboratory, Curvularia-infected plants were able to grow at soil temperatures of 65 °C (149 °F)! Interestingly, neither fungus nor plant could grow alone at temperatures above 38 °C. As if this story was not interesting enough, the most recent work by Marquez and colleagues (2007) has shown that the ability of the fungus to confer heat resistance is in turn dependent on the presence of a naturally occurring virus inside the fungal hyphae. Fungi cured of this virus were unable to confer heat resistance to their host plant, while fungi re-infected with the virus performed as per normal.
The second example comes from a plant-pathogen interaction between fungal species in the genus Rhizopus that can infect and kill rice seedlings. The ability of the fungus to successfully parasitize its host depends on the synthesis of a substance called rhizoxin, which helps in the fungal attack by inhibiting mitosis of host plant cells. Partida-Martinez and Hertweck (2005) were initially interested in the production of rhizoxin but were puzzled when they were unable to find genes related to its production in the genome of the fungus. Surprisingly though, they did find candidate genes for rhizoxin biosynthesis, but these genes appeared to be bacterial in origin. Closer inspection revealed the presence of live bacterial cells living within the fungal hyphae (see accompanying photograph). In a series of elegant experiments, Hertweck and colleagues demonstrated conclusively that rhizoxin is actually synthesized by endosymbiotic bacteria in the genus Burkholderia and that fungal strains without these bacteria are unable to synthesize rhizoxin. Further research by the same group has shown that this symbiosis has become so central to the fungus that it will not sporulate in the absence of its bacterial symbiont (Partida- Martinez et al. 2007). Intriguingly, evolutionary evidence suggests that the symbiosis between Rhizopus and Burkholderia was possible only after the fungus itself evolved resistance to rhizoxin, and raises the possibility that this is a case of old enemies turned to cooperation (Schmitt et al. 2008).
We are just beginning to look for these types of interactions, yet the evidence so far suggests that they may be fairly common. For example, endosymbiotic bacteria have also been observed in the hyphae of arbuscular mycorrhizal fungi, although their function is still not known. Unraveling these complex interactions will require good science, but as these two studies have shown, the rewards are well worth the trouble.
- Partida-Martinez L.P. & Hertweck C. (2005). Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature, 437, 884-888. (Abstract)
- Marquez L.M., Redman R.S., Rodriguez R.J. & Roossinck M.J. (2007). A virus in a fungus in a plant: Three-way symbiosis required for themal tolerance. Science, 315, 513-515. (Abstract)
- Partida-Martinez L.P., Monajembashi S., Greulich K.O., & Hertweck C. (2007) Endosymbiont-Dependent Host Reproduction Maintains Bacterial-Fungal Mutualism. Current Biology, 17, 773-777. (PDF)
- Schmitt I., Partida-Martinez L.P., Winkler R., Voigt K., Einax E., Dolz F., Telle S., Wostemeyer J. & Hertweck C. (2008). Evolution of host restistance in a toxin-producing bacterial-fungal alliance. Isme Journal, 2, 632-641. (PDF)