Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants

Abstract

Symbiont choice has been proposed to play an important role in shaping many symbiotic relationships, including the fungus-growing ant-microbe mutualism. Over millions of years, fungusgrowing ants have defended their fungus gardens from specialized parasites with antibiotics produced by an actinomycete bacterial mutualist (genus Pseudonocardia). Despite the potential of being infected by phylogenetically diverse strains of parasites, each ant colony maintains only a single Pseudonocardia symbiont strain, which is primarily vertically transmitted between colonies by the founding queens. In this study, we show that Acromyrmex leaf-cutter ants are able to differentiate between their native actinomycete strain and a variety of foreign strains isolated from sympatric and allopatric Acromyrmex species, in addition to strains originating from other fungusgrowing ant genera. The recognition mechanism is sufficiently sensitive for the ants to discriminate between closely related symbiont strains. Our findings suggest that symbiont recognition may play a crucial role in the fungus-growing ant-bacterium mutualism, likely allowing the ants to retain ecological flexibility necessary for defending their garden from diverse parasites and, at the same time, resolve potential conflict that can arise from rearing competing symbiont strains.

Rethinking crop-disease management in fungus-growing ants

“…Extrapolations from rather limited data collected Ϸ10 years ago now appear to be oversimplifications in need of more explicit testing and at least partial rectification, a process that was already initiated less explicitly a few years ago (13). This changing insight mirrors the way in which we obtained our current view on coevolution between the higher attine ants and their garden symbionts.…”

“…In addition, their in vitro agar plate encounters often end up with the crop symbiont being inhibited or killed by the actinomycete strains, suggesting that the ants need to apply actinomycete-produced antibiotics with surgical precision and in doses that strictly match the infection problem. However, the pairings used were random, so this evidence does not preclude that natural combinations of resident symbionts in field colonies are better matched (13).…”

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

“…A finding of specificity at finer phylogenetic levels is also supported by permutation tests of non-random patterns of Pseudonocardia association by ant genus (see electronic supplementary material, table S2). This pattern of specificity suggests that exchanges of Pseudonocardia between colonies of fungus-growing ants may be restricted by ant-bacterial incompatibility, potentially mediated by (i) glandular secretions in the ants [23] and/or (ii) behavioural recognition of Pseudonocardia by worker (known in Acromyrmex: [47]). …”

Partner choice and fidelity stabilize coevolution in a Cretaceous-age defensive symbiosis

“…Although such a pattern is also observed for some extracellular symbioses with especially tight host-symbiont integration (14,15), the ability of many extracellularly transmitted symbionts to spend part of their life cycle outside of the host's body is often reflected in more or less extensive horizontal transmission or de novo acquisition of symbionts from the environment (16,17). In these cases, partner choice mechanisms are expected to ensure specificity in the establishment and maintenance of the association (18). The nature of such control mechanisms, however, remains poorly understood.…”