Symbiosis and Dysbiosis in fungus - gardening ants: ants drive microbiome structure and homeostasis of fungal symbionts
One of the most important evolutionary transitions is the cooperation of vastly unrelated species (symbiosis). What stabilizes symbiotic associates or causes their collapse (dysbiosis) is a mystery. Recent advances due to high throughput sequencing techniques indicate that most symbioses (and eukaryotic organisms) are in fact communities of interacting bacteria, fungi in addition to macroscopic hosts and symbionts. Fungus-gardening (attine) ants have had a symbiotic relationship with specific fungal lineages for millions of years. These ants are excellent model systems for exploring the basis of specificity as the host and symbionts are macroscopic and can be easily experimentally manipulated. The most derived attine ants (the "higher attines") typically grow two broad clades of fungi. Most ants in the genus Trachymyrmex tend to grow Clade-B fungi, which are a group of undescribed Leucoagaricus species, whereas the leaf-cutting ants in the genera Acromyrmex and Atta tend to grow Clade-A fungi (Leucoagaricus gongylophorus). However, there are some species of Trachymyrmex that are known to grow Clade-A fungi and some leaf-cutting ants that grow Clade-B fungi. Previous work has shown switching the cultivar grown by Trachymyrmex septentrionalis ants, from Clade-B to Clade-A fungus, creates an unstable symbiosis between the ants and their grown cultivar, so that a sudden and catastrophic decrease in the size of their fungal garden invariably results. One hypothesis is that the stability of ant-fungal combinations is maintained by interactions among members of the microbiome of fungus-gardening ants and their fungus gardens. We explored whether changing fungal partners impacts the microbiomes of the host ants and their symbiotic fungus by performing cross fostering experiments that forced ants to grow novel fungi. Specifically, these experiments forced ants of two Trachymyrmex species (T. pomonae and T. septentrionalis ) that normally grow Clade-B fungi to grow Clade-A fungi and compared these to a species that is known to growth both Clade-A and Clade-B (T. arizonensis). The experiments revealed that Trachymyrmex ants altered their novel Clade-A garden microbiomes and that these were similar to that of the "control or sham switched" Clade-B fungus gardens. These results suggest that ants play a role in determining the structure of the microbiome of their fungus gardens. Since these combinations are not stable, it is possible that the "novel" microbiome structured by the Trachymyrmex ants is a factor in driving symbiotic collapse. Such findings suggest each fungal clade may have specificity with assorted bacterial communities.