Abstract

BackgroundLeaf-cutter ants use fresh plant material to grow a mutualistic fungus that serves as the ants' primary food source. Within fungus gardens, various plant compounds are metabolized and transformed into nutrients suitable for ant consumption. This symbiotic association produces a large amount of refuse consisting primarily of partly degraded plant material. A leaf-cutter ant colony is thus divided into two spatially and chemically distinct environments that together represent a plant biomass degradation gradient. Little is known about the microbial community structure in gardens and dumps or variation between lab and field colonies.Methodology/Principal FindingsUsing microbial membrane lipid analysis and a variety of community metrics, we assessed and compared the microbiota of fungus gardens and refuse dumps from both laboratory-maintained and field-collected colonies. We found that gardens contained a diverse and consistent community of microbes, dominated by Gram-negative bacteria, particularly γ-Proteobacteria and Bacteroidetes. These findings were consistent across lab and field gardens, as well as host ant taxa. In contrast, dumps were enriched for Gram-positive and anaerobic bacteria. Broad-scale clustering analyses revealed that community relatedness between samples reflected system component (gardens/dumps) rather than colony source (lab/field). At finer scales samples clustered according to colony source.Conclusions/SignificanceHere we report the first comparative analysis of the microbiota from leaf-cutter ant colonies. Our work reveals the presence of two distinct communities: one in the fungus garden and the other in the refuse dump. Though we find some effect of colony source on community structure, our data indicate the presence of consistently associated microbes within gardens and dumps. Substrate composition and system component appear to be the most important factor in structuring the microbial communities. These results thus suggest that resident communities are shaped by the plant degradation gradient created by ant behavior, specifically their fungiculture and waste management.

Highlights

  • Leaf-cutter ants (Atta and Acromyrmex: Tribe Attini) are the most phylogenetically derived members of a monophyletic group of Neotropical ants that cultivate specialized fungal symbionts that serve as the colony’s primary food source

  • Colonies can harvest a large amount of plant material, for example a study of Atta colombica colonies in Panama found that they collected an average of,250 Kg of plant material per colony during a one-year observation period [9,10]

  • Richness analysis indicated that gardens were well sampled, and that richness was similar between lab and field fungus gardens

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Summary

Introduction

Leaf-cutter ants (Atta and Acromyrmex: Tribe Attini) are the most phylogenetically derived members of a monophyletic group of Neotropical ants that cultivate specialized fungal symbionts that serve as the colony’s primary food source. Leaf-cutters are unique in that they exclusively use fresh plant material to cultivate their fungal mutualist [1,2,3,4]. The ants protect their fungal cultivar from pathogens and parasites [3,5,6,7], provide the fungus with a constant source of nutrients [3,4], and aid in its growth and dispersal [3]. Little is known about the microbial community structure in gardens and dumps or variation between lab and field colonies

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