Abstract
The attine ants of South and Central America are ancient farmers, having evolved a symbiosis with a fungal food crop >50 million years ago. The most evolutionarily derived attines are the Atta and Acromyrmex leafcutter ants, which harvest fresh leaves to feed their fungus. Acromyrmex and many other attines vertically transmit a mutualistic strain of Pseudonocardia and use antifungal compounds made by these bacteria to protect their fungal partner against co-evolved fungal pathogens of the genus Escovopsis. Pseudonocardia mutualists associated with the attines Apterostigma dentigerum and Trachymyrmex cornetzi make novel cyclic depsipeptide compounds called gerumycins, while a mutualist strain isolated from derived Acromyrmex octospinosus makes an unusual polyene antifungal called nystatin P1. The novelty of these antimicrobials suggests there is merit in exploring secondary metabolites of Pseudonocardia on a genome-wide scale. Here, we report a genomic analysis of the Pseudonocardia phylotypes Ps1 and Ps2 that are consistently associated with Acromyrmex ants collected in Gamboa, Panama. These were previously distinguished solely on the basis of 16S rRNA gene sequencing but genome sequencing of five Ps1 and five Ps2 strains revealed that the phylotypes are distinct species and each encodes between 11 and 15 secondary metabolite biosynthetic gene clusters (BGCs). There are signature BGCs for Ps1 and Ps2 strains and some that are conserved in both. Ps1 strains all contain BGCs encoding nystatin P1-like antifungals, while the Ps2 strains encode novel nystatin-like molecules. Strains show variations in the arrangement of these BGCs that resemble those seen in gerumycin gene clusters. Genome analyses and invasion assays support our hypothesis that vertically transmitted Ps1 and Ps2 strains have antibacterial activity that could help shape the cuticular microbiome. Thus, our work defines the Pseudonocardia species associated with Acromyrmex ants and supports the hypothesis that Pseudonocardia species could provide a valuable source of new antimicrobials.
Highlights
Almost all antibiotics currently in clinical use are derived from the secondary metabolites of a group of soil bacteria called actinomycetes, but the discovery of these strains and their natural products (NPs) peaked in the 1950s
The large callow workers of A. echinatior are covered in filamentous Pseudonocardia that are visible as a whitish covering on the cuticle (Figure 1) and can be cultured on nutrient agar
The A. echinatior workers typically have a concentration of Pseudonocardia on their laterocervical plates, so we scraped the plates of 1–2 workers taken from 23 separate A. echinatior colonies to isolate their mutualist strains
Summary
Almost all antibiotics currently in clinical use are derived from the secondary metabolites of a group of soil bacteria called actinomycetes, but the discovery of these strains and their natural products (NPs) peaked in the 1950s. Genome mining for novel BGCs in soil actinomycetes isolated over the last 80 years, plus new actinomycete strains isolated from under-explored environments, promises to yield 1000s of new NPs, including new anti-infective drugs (Katz and Baltz, 2016). One promising new approach is to genome mine strains that have co-evolved with their eukaryotic hosts Such symbiotic relationships are known as protective mutualisms, because the plant or animal host houses, feeds, and sometimes vertically transmits the bacteria in exchange for antibiotics that protect them against infection (Clardy et al, 2009; Kaltenpoth, 2009; Seipke et al, 2011b). One of the best characterized examples are the protective mutualisms between the attine ants of South and Central America and their vertically transmitted strains of Pseudonocardia (Cafaro et al, 2011; Caldera and Currie, 2012)
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