Low Virulence of the Fungi Escovopsis and Escovopsioides to a Leaf-Cutting Ant-Fungus Symbiosis

Eusocial insects interact with a diversity of parasites that can threaten their survival and reproduction. The amount of harm these parasites cause to their hosts (i.e., their virulence) can be influenced by numerous factors, such as the ecological context in which the parasite and its host are inserted. Leaf-cutting ants (genera Atta, Acromyrmex and Amoimyrmex, Attini: Formicidae) are an example of a eusocial insect whose colonies are constantly threatened by parasites. The fungi Escovopsis and Escovopsioides (Ascomycota: Hypocreales) are considered a highly virulent parasite and an antagonist, respectively, to the leaf-cutting ants’ fungal cultivar, Leucoagaricus gongylophorus (Basidiomycota: Agaricales). Since Escovopsis and Escovopsioides are common inhabitants of healthy colonies that can live for years, we expect them to have low levels of virulence. However, this virulence could vary depending on ecological context. We therefore tested two hypotheses: (i) Escovopsis and Escovopsioides are of low virulence to colonies; (ii) virulence increases as colony complexity decreases. For this, we used three levels of complexity: queenright colonies (fungus garden with queen and workers), queenless colonies (fungus garden and workers, without queen) and fungus gardens (without any ants). Each was inoculated with extremely high concentrations of conidia of Escovopsis moelleri, Escovopsioides nivea, the mycoparasitic fungus Trichoderma longibrachiatum or a blank control. We found that these fungi were of low virulence to queenright colonies. The survival of queenless colonies was decreased by E. moelleri and fungus gardens were suppressed by all treatments. Moreover, E. nivea and T. longibrachiatum seemed to be less aggressive than E. moelleri, observed both in vivo and in vitro. The results highlight the importance of each element (queen, workers and fungus garden) in the leaf-cutting ant-fungus symbiosis. Most importantly, we showed that Escovopsis may not be virulent to healthy colonies, despite commonly being described as such, with the reported virulence of Escovopsis being due to poor colony conditions in the field or in laboratory experiments.

The ant fungus garden acts as an external digestive system

Most animals digest their food within their own bodies, but some do not. Many species of ants grow fungus gardens that pre-digest food as an essential step of the ants’ nutrient uptake. To better understand this digestion process, we generated a 3D molecular map of an Atta texana fungus garden, revealing chemical modifications mediated by the fungus garden as plant material passes through.

Metagenomics reveals diet-specific specialization of bacterial communities in fungus gardens of grass- and dicot-cutter ants

Leaf-cutter ants in the genusAttaare dominant herbivores in the Neotropics. While most species ofAttacut dicots to incorporate into their fungus gardens, some species specialize on grasses. Here we examine the bacterial community associated with the fungus gardens of grass- and dicot-cutter ants to examine how changes in substrate input affect the bacterial community. We sequenced the metagenomes of 12Attafungus gardens, across four species of ants, with a total of 5.316 Gbp of sequence data. We show significant differences in the fungus garden bacterial community composition between dicot- and grass-cutter ants, with grass-cutter ants having lower diversity. Reflecting this difference in community composition, the bacterial functional profiles between the fungus gardens are significantly different. Specifically, grass-cutter ant fungus garden metagenomes are particularly enriched for genes responsible for amino acid, siderophore, and terpenoid biosynthesis while dicot-cutter ant fungus gardens metagenomes are enriched in genes involved in membrane transport. These differences in bacterial community composition and functional capacity show that different substrate inputs matter for fungus garden bacteria, and sheds light on the potential role of bacteria in mediating the ants’ transition to the use of a novel substrate.

The interactions of ants with their biotic environment

This s pecial feature results from the symposium ‘Ants 2016: ant interactions with their biotic environments’ held in Munich in May 2016 and deals with the interactions between ants and other insects, plants, microbes and fungi, studied at micro- and macroevolutionary levels with a wide range of approaches, from field ecology to next-generation sequencing, chemical ecology and molecular genetics. In this paper, we review key aspects of these biotic interactions to provide background information for the papers of this s pecial feature . After listing the major types of biotic interactions that ants engage in, we present a brief overview of ant/ant communication, ant/plant interactions, ant/fungus symbioses, and recent insights about ants and their endosymbionts. Using a large molecular clock-dated Formicidae phylogeny, we map the evolutionary origins of different ant clades' interactions with plants, fungi and hemiptera. Ants' biotic interactions provide ideal systems to address fundamental ecological and evolutionary questions about mutualism, coevolution, adaptation and animal communication.

Ant-fungus Interactions: Laboulbenia camponoti Batra in Italy and a New Host for L. formicarum Thaxter (Fungi: Ascomycota, Laboulbeniales)

One Laboulbenia species is added to the checklist of Italian fungi. Laboulbenia camponoti was detected on the ant Camponotus aethiops. Additionally, L. formicarum was found on a new host (Lasius niger) in France. An updated map of world distribution for the two Laboulbenia is presented. Based on present knowledge, L. camponoti shows a much higher structural and phylogenetic host specificity than L. formicarum.

Draft Genome Sequence of the Ant-Associated Fungus Phialophora attae (CBS 131958)

The black yeast Phialophora attae was isolated from the cuticle of tropical ant gynes. The ant-fungus association is sustained due to symbiotic evolutionary adaptations that allow fungal assimilation and tolerance of toxic compounds produced by the ant. The genome sequence of the first ant-associated fungus, P. attae , is presented here.