Actinomycetes inhibit filamentous fungi from the cuticle of Acromyrmex leafcutter ants

Abstract

Actinomycetes bacteria associated with leafcutter ants produce secondary metabolites with antimicrobial properties against Escovopsis, a fungus specialized in attacking the gardens of fungus-growing ants, which denies the ants their food source. Because previous studies have used fungi isolated from fungus gardens but not from ant integument, the aims of the present study were to isolate actinomycetes associated with the cuticle of the Acromyrmex spp. and to quantify their inhibition abilities against the filamentous fungal species carried by these ants. The results demonstrated that actinomycetes had varied strain-dependent effects on several filamentous fungal species in addition to antagonistic activity against Escovopsis. The strain isolated from Acromyrmex balzani was identified as a Streptomyces species, whereas the remaining isolates were identified as different strains belonging to the genus Pseudonocardia. These findings corroborate the hypothesis that actinomycetes do not act specifically against Escovopsis mycoparasites and may have the ability to inhibit other species of pathogenic fungi.

Effects of entomopathogenic fungi on the mortality and immune system of the leaf‐cutting ant Acromyrmex subterraneus subterraneus

“…Inhibition tests in Petri dishes using A. ochraceus (among other fungal species) and five lineages of Pseudonocardia bacteria, one of which originated from the present work, showed that the controls exhibited greater average growth that differed significantly from that of the treated ants (Dângelo et al, 2016). This was verified by the formation of an inhibition halo caused by the antimicrobial substances produced by the bacteria.…”

Pseudonocardia Symbionts of Fungus-Growing Ants and the Evolution of Defensive Secondary Metabolism

“…Increased abundance of Pseudonocardia on ants in response to parasite infection underscores the predicted function of this bacterium in the system: to protect the fungal cultivar against Escovopsis (Currie et al, 1999b(Currie et al, , 2003a. Pseudonocardia prevent Escovopsis infections of ant fungus gardens in vivo (Currie et al, 2003a;Little and Currie, 2008;Poulsen et al, 2010), and Pseudonocardia isolates consistently inhibit Escovopsis cultures in vitro (Currie et al, 1999b(Currie et al, , 2003aSchoenian et al, 2011;Meirelles et al, 2013;Sit et al, 2015;Dângelo et al, 2016). Some researchers have therefore suggested that these symbionts co-evolve with one another, locked in an arms race where Pseudonocardia and Escovopsis constantly evolve new mechanisms to gain an advantage over each other (Woolhouse et al, 2002).…”

“…However, Pseudonocardia defenses against Escovopsis can vary (Poulsen et al, 2010), and some fungus-growing ants are not pathogenized by Escovopsis (Rodrigues et al, 2008), despite hosting Pseudonocardia. Further studies have shown that Pseudonocardia isolates have broad-spectrum activities against fungi other than just Escovopsis (Sen et al, 2009;Meirelles et al, 2013;Dângelo et al, 2016), suggesting that Pseudonocardia's antimicrobials inhibit diverse pathogens in the fungus-growing ant symbiosis.…”

“…One hypothesis is that actinomycetes other than Pseudonocardia are also maintained as defensive symbionts of ants. Several studies have isolated such actinomycetes from fungus-growing ants and showed that they inhibit fungal pathogens in vitro (Kost et al, 2007;Mueller et al, 2008;Haeder et al, 2009;Sen et al, 2009;Barke et al, 2010;Dângelo et al, 2016). Schoenian et al (2011) also found compounds known to be produced by Streptomyces strains on the cuticle of Acromyrmex ants, concluding that those actinomycetes were therefore ant symbionts.…”

Molecules to Ecosystems: Actinomycete Natural Products In situ

“…These actinomycetes were studied in assays against invading fungal species and were found to produce a suite of antifungals including antimycins, candicidin, dentigerumycin, and nystatin variants which suppress Escovopsis and other potential pathogens while leaving L. gongylophorus unharmed (Haeder et al, 2009; Seipke et al, 2012; Dângelo et al, 2016). More recently, Sit et al (2015) discovered, and chemically characterized, new antifungals related to dentigerumycin, called gerumycins, synthesized by Pseudonocardia spp.…”