Interaction specificity between leaf-cutting ants and vertically transmitted Pseudonocardia bacteria

Abstract

BackgroundThe obligate mutualism between fungus-growing ants and microbial symbionts offers excellent opportunities to study the specificity and stability of multi-species interactions. In addition to cultivating fungus gardens, these ants have domesticated actinomycete bacteria to defend gardens against the fungal parasite Escovopsis and possibly other pathogens. Panamanian Acromyrmex echinatior leaf-cutting ants primarily associate with actinomycetes of the genus Pseudonocardia. Colonies are inoculated with one of two vertically transmitted phylotypes (Ps1 or Ps2), and maintain the same phylotype over their lifetime. We performed a cross-fostering experiment to test whether co-adaptations between ants and bacterial phylotypes have evolved, and how this affects bacterial growth and ant prophylactic behavior after infection with Escovopsis.ResultsWe show that Pseudonocardia readily colonized ants irrespective of their colony of origin, but that the Ps2 phylotype, which was previously shown to be better able to maintain its monocultural integrity after workers became foragers than Ps1, reached a higher final cover when grown on its native host than on alternative hosts. The frequencies of major grooming and weeding behaviors co-varied with symbiont/host combinations, showing that ant behavior also was affected when cuticular actinomycete phylotypes were swapped.ConclusionThese results show that the interactions between leaf-cutting ants and Pseudonocardia bear signatures of mutual co-adaptation within a single ant population.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0308-2) contains supplementary material, which is available to authorized users.

Genome Analysis of Two Pseudonocardia Phylotypes Associated with Acromyrmex Leafcutter Ants Reveals Their Biosynthetic Potential

“…We consistently isolated either a single Ps1 or Ps2 Pseudonocardia strain from 22 out of the 23 ant colonies but for colony Ae_707, the only colony reared in Norwich rather than Copenhagen, we isolated both Ps1 and Ps2 strains. This result matched an earlier survey (Andersen et al, 2015), which had a single double infection in a sample of 19 colonies of Panamanian A. echinatior and A. octospinosus . In total, we isolated 24 strains of Pseudonocardia .…”

“…Not only are the two phylotypes shared between congener ant species, they are also consistently found in ca. 50/50 frequencies across colonies (Andersen et al, 2015), and this is reflected in our genome sequencing of strains for the present study. This is a remarkable natural distribution in light of the findings we present here on how different the two strains are at the genome level.…”

“…In total, we isolated 24 strains of Pseudonocardia . We then selected five Ps1 strains and five Ps2 strains for genome sequencing ( Table 1 ); these included six strains originating from colonies also used in the Andersen et al (2015) study. Under laboratory culture conditions, Ps2 strains generally grew faster and generated more biomass than Ps1 strains, but all the Pseudonocardia isolates grew weakly compared to Streptomyces species and to Pseudonocardia strains isolated previously from A. octospinosus worker ants (Barke et al, 2010).…”

“…The two Pseudonocardia phylotypes were first recognized as distinct more than 10 years ago and were subsequently found to be shared by sympatric populations of A. echinatior and A. octospinosus in Panama (Poulsen et al, 2005; Andersen et al, 2015) and A. volcanus (Sapountzis et al, 2015). Not only are the two phylotypes shared between congener ant species, they are also consistently found in ca.…”

“…Little is known about these strains, but previous studies have found clear differences between Ps1 and Ps2 at the 16S rRNA gene level (Poulsen et al, 2005). Also, older worker ants carrying a Ps1 strain are associated with a more diverse host cuticular microbiome than those carrying Ps2 (Andersen et al, 2013), and there are some colony-level behavioral differences in the ant hosts that are related to disease control performance (Andersen et al, 2015). We reasoned this could be due to differences in the Pseudonocardia symbiont growth rates, the antibiotics they encode, or both, and this prompted us to investigate the differences between the genomes of the two phylotypes.…”