Abstract
Actinobacteria belonging to the genus Pseudonocardia have evolved a close relationship with multiple species of fungus-growing ants, where these bacteria produce diverse secondary metabolites that protect the ants and their fungal mutualists from disease. Recent research has charted the phylogenetic diversity of this symbiosis, revealing multiple instances where the ants and Pseudonocardia have formed stable relationships in which these bacteria are housed on specific regions of the ant’s cuticle. Parallel chemical and genomic analyses have also revealed that symbiotic Pseudonocardia produce diverse secondary metabolites with antifungal and antibacterial bioactivities, and highlighted the importance of plasmid recombination and horizontal gene transfer for maintaining these symbiotic traits. Here, we propose a multi-level model for the evolution of Pseudonocardia and their secondary metabolites that includes symbiont transmission within and between ant colonies, and the potentially independent movement and diversification of their secondary metabolite biosynthetic genes. Because of their well-studied ecology and experimental tractability, Pseudonocardia symbionts of fungus-growing ants are an especially useful model system to understand the evolution of secondary metabolites, and also comprise a significant source of novel antibiotic and antifungal agents.
Highlights
Actinomycete bacteria form many beneficial symbioses with eukaryotes, where the host typically provides nutritional support and the actinomycetes provide chemical defense (Van Arnam et al, 2018)
Pseudonocardia symbionts of Apterostigma dentigerum ants have population structures that are consistent with vertical transmission between their dispersallimited hosts (Caldera and Currie, 2012; Mcdonald et al, 2019), but similar population structures were not detected for Pseudonocardia symbionts of Trachymyrmex septentrionalis ants using methods with lower phylogenetic resolution (Mikheyev et al, 2008)
Ants can recognize their native Pseudonocardia symbiont (Zhang et al, 2007; Poulsen et al, 2011), and experimental symbiont swaps decrease symbiont abundance and ant grooming behavior, thereby allowing increased pathogen infection (Armitage et al, 2011; Andersen et al, 2015). These results show that Pseudonocardia can be adapted to their specific ant hosts and vice versa, as expected from a predominantly vertical mode of transmission, symbiont replacement remains possible
Summary
Actinomycete bacteria form many beneficial symbioses with eukaryotes, where the host typically provides nutritional support and the actinomycetes provide chemical defense (Van Arnam et al, 2018). The best-studied of these are insect-actinomycete mutualisms, which are widespread and the source of many novel secondary metabolites with antibacterial and antifungal activity (Chevrette and Currie, 2019). Insect-associated Streptomyces inhibited clinically relevant microbes more effectively than soil-isolated Streptomyces (Chevrette et al, 2019), perhaps due to co-evolution between insects and microbes that has selected for defensive metabolites inhibiting pathogens but not their hosts (Clardy et al, 2009). The potential rise of antimicrobial resistance in these symbioses must have been overcome by selection consistently replenishing and diversifying their defensive metabolites. Few systems exist where such ecological and evolutionary dynamics have been dissected in detail
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