Symbiosis and dysbiosis in fungus-gardening ants: A microbiome approach

One of the most important evolutionary transitions is the cooperation of vastly unrelated species (symbiosis). The mechanisms that stabilize symbioses or causes collapse (dysbiosis) are likely complex, yet unknown in most cases. 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. Each of the members are often providing goods and services with other members. We describe the bacterial microbiomes of fungus gardening ants and their symbiotic fungi that result when ants grow novel fungi. Specifically, we describe bacterial microbiome changes when three species of Trachymyrmex ants are forced to grow either so-called ‘Clade A’ fungi (Leucocoprinus gongylophorus) or ‘Clade B’ fungi (Leucocoprinus sp.). Earlier studies have demonstrated that two of these species (T. septentrionalis and T. pomonae) experience sudden losses of fungus gardens when forced to grow Clade A fungi, whereas T. arizonensis is known to grow either fungal lineage in nature that are known to form stable associations for several years in the laboratory. Bacterial microbiome changes that resulted from growing either fungal species were most pronounced in the fungus gardens. Ants that exhibited ‘dysbiosis’ experienced significant reductions in nitrogen fixing bacteria and increases in Mollicute bacteria (Mesoplasma and/or Spiroplasma) that are thought to be involved amino acid and carbohydrate metabolism. As a result, it would appear that symbiont switching is constrained in nature, in part, by disruptions in nutritional pathways among ants, fungal symbiont and bacterial associates.