Specificity in the symbiotic association between fungus-growing ants and protective Pseudonocardia bacteria

Abstract

Fungus-growing ants (tribe Attini) engage in a mutualism with a fungus that serves as the ants' primary food source, but successful fungus cultivation is threatened by microfungal parasites (genus Escovopsis). Actinobacteria (genus Pseudonocardia) associate with most of the phylogenetic diversity of fungus-growing ants; are typically maintained on the cuticle of workers; and infection experiments, bioassay challenges and chemical analyses support a role of Pseudonocardia in defence against Escovopsis through antibiotic production. Here we generate a two-gene phylogeny for Pseudonocardia associated with 124 fungusgrowing ant colonies, evaluate patterns of ant -Pseudonocardia specificity and test Pseudonocardia antibiotic activity towards Escovopsis. We show that Pseudonocardia associated with fungus-growing ants are not monophyletic: the ants have acquired free-living strains over the evolutionary history of the association. Nevertheless, our analysis reveals a significant pattern of specificity between clades of Pseudonocardia and groups of related fungus-growing ants. Furthermore, antibiotic assays suggest that despite Escovopsis being generally susceptible to inhibition by diverse Actinobacteria, the ant-derived Pseudonocardia inhibit Escovopsis more strongly than they inhibit other fungi, and are better at inhibiting this pathogen than most environmental Pseudonocardia strains tested. Our findings support a model that many fungus-growing ants maintain specialized Pseudonocardia symbionts that help with garden defence.

Selvamicin, an atypical antifungal polyene from two alternative genomic contexts

“…In contrast, the whole genomes differ more substantially. The average nucleotide identity (27) calculated across conserved replicons on both chromosomes is only 83% and a comparison of housekeeping gene sequences places LS1 and LS2 into distinct clades previously established for ant-associated Pseudonocardia (28,29). Overall, the two BGCs are much more similar to one another than are their bacterial hosts.…”

Anthropogenic effects on interaction outcomes: examples from insect-microbial symbioses in forest and savanna ecosystems

“…In addition to employing behavioral defenses to physically remove Escovopsis from infected garden material (Currie and Stuart 2001;Abramowski et al 2011), the ants employ defensive mutualists to control Escovopsis. These are Pseudonocardia bacteria (Actinomycetales: Pseudonocardiaceae) (Currie et al 1999b;Cafaro and Currie 2005) that are maintained on the cuticle of the ant host where they secrete secondary metabolites that strongly inhibit Escovopsis (Currie et al 2006;Oh et al 2009;Poulsen et al 2010;Cafaro et al 2011). Experiments where Pseudonocardia has been removed have resulted in subsequent Escovopsis infection (Currie et al 2003a).…”

“…Fungus-growing ants, the cultivar fungus, the parasites of the fungus, and the defensive Pseudonocardia mutualists have all undergone some degree of co-diversification, and possibly coevolution (Mueller et al 1998;Currie et al 2003b;Cafaro et al 2011). The two best-studied mutualistic symbionts, the cultivar and Pseudonocardia, are both vertically transmitted between host-ant generations by default (von Ihering 1898; Autuori 1956;Currie et al 1999b;Mueller et al 2001;Fernández-Marín et al 2004), leading to expectations of patterns of host-mutualist cocladogenesis, which indeed is observed.…”

Genome Sequence of the 1,4-Dioxane-Degrading Pseudonocardia dioxanivoransStrain CB1190

“…Pseudonocardia represents a genus of bacteria with diverse niches, from free-living microorganisms capable of degrading xenobiotic compounds (5-8, 15, 17) to the antibiotic-producing symbionts of fungus-farming ants (1,2,13,20). Strain CB1190 was chosen for sequencing by the U.S. Department of Energy Joint Genome Institute (JGI) to gain insight into 1,4-dioxane metabolism, as well as to learn about general carbon and nitrogen metabolism in the genus.…”