Ants manage polyol production to fight fungal antagonists

The attinas, ants of the Attina subtribe (Formicidae: Myrmicinae), colonize vast areas in the American continent. This impressive fitness depends on culturing mutualistic fungi in their "fungus gardens" to digest biomass. Atta bisphaerica, a derived leafcutter attina, degrades plant biomass into polyols in their fungus gardens. The proposed strategic use of polyols to accumulate energy and preserve digestive fungal exoenzymes is a fascinating evolutionary development in ants. We found that polyol production is a conserved trait among derived and less derived attinas. However, Leucoagaricus gongylophorus, the mutualistic fungus of the more derived leafcutter ants, expresses an incomplete set of enzymes necessary to reduce carbohydrates to polyols compared to Leucocoprinus sp., the mutualistic fungus of less derived ants. Although ants search for and consume these polyols with lower priority than glucose, polyols are important for developing and sporulating antagonistic fungi living in the fungus gardens. Therefore, despite the massive and widespread production by the fungus garden and the proposed benefits, polyols do not attract or preferentially feed the ants but stimulate invading fungi. Thus, the production of polyols was not a decisive factor in attracting ants to establish mutualism with fungi but rather in spreading fungi that can threaten ant colonies. Ants' evolution mitigated this setback by increasing by-product diversity, minimizing polyol concentration, and switching to mutualistic fungi lacking the expression of critical enzymes for polyol biosynthesis.IMPORTANCEMicrobial communities are critical elements of biodiversity modulating life on Earth. Insects interact intensely with microorganisms to obtain nutrients. They also suffer from diseases caused by microbial infections. The present study is an example of how the different actors of a microbial community interact with each other and their insect hosts. We found that polyols produced by microbes that digest plant matter affect nutrition and facilitate infections in leafcutter ants. This knowledge is crucial for understanding ant-microbe interaction and controlling agricultural pest leafcutter ants.