High Diversity and Low Specificity of Chaetothyrialean Fungi in Carton Galleries in a Neotropical Ant–Plant Association

Abstract

New associations have recently been discovered between arboreal ants that live on myrmecophytic plants, and different groups of fungi. Most of the – usually undescribed – fungi cultured by the ants belong to the order Chaetothyriales (Ascomycetes). Chaetothyriales occur in the nesting spaces provided by the host plant, and form a major part of the cardboard-like material produced by the ants for constructing nests and runway galleries. Until now, the fungi have been considered specific to each ant species. We focus on the three-way association between the plant Tetrathylacium macrophyllum (Salicaceae), the ant Azteca brevis (Formicidae: Dolichoderinae) and various chaetothyrialean fungi. Azteca brevis builds extensive runway galleries along branches of T. macrophyllum. The carton of the gallery walls consists of masticated plant material densely pervaded by chaetothyrialean hyphae. In order to characterise the specificity of the ant–fungus association, fungi from the runway galleries of 19 ant colonies were grown as pure cultures and analyzed using partial SSU, complete ITS, 5.8S and partial LSU rDNA sequences. This gave 128 different fungal genotypes, 78% of which were clustered into three monophyletic groups. The most common fungus (either genotype or approximate species-level OTU) was found in the runway galleries of 63% of the investigated ant colonies. This indicates that there can be a dominant fungus but, in general, a wider guild of chaetothyrialean fungi share the same ant mutualist in Azteca brevis.

A phylogenetic perspective on the association between ants (Hymenoptera: Formicidae) and black yeasts (Ascomycota: Chaetothyriales)

“…A highly illustrative example is a monophyletic clade in the Trichomeriaceae composed of closely related strains from Central American Azteca (Dolichoderinae) plant-ants on Cecropia (Urticaceae) and Tetrathylacium (Salicaceae) (domatia and carton fungi), southeast Asian Cladomyrma (Formicinae) plant-ants on Saraca (Fabaceae) (domatia fungi) and African Crematogaster (Myrmicinae) (carton fungi) (figure 1). Phylogenies based on subsets of strains (figure 2) and computation of ITS sequence similarity revealed seven cases-two of which had already been noted by Nepel et al [15]-of a single MOTU (more than 99% ITS sequence similarity) comprised of strains isolated from several ant species and/or on several continents. One MOTU (strain T394 from Nepel et al [15] and MCRE12) was found in carton nests of Crematogaster sp.…”

“…Ant-associated Chaetothyriales can be classified into three main functional groups: (i) strains associated with fungus-growing attine ants [10][11][12]; (ii) strains involved in 'carton' structures built by ants [7,[13][14][15]; and (iii) strains associated with ant-plant symbioses [7,16]. The first group, Chaetothyriales associated with attine ants, are not the focus of our study.…”

“…Botryosphaeriales, Eurotiales, Capnodiales, Chaetothyriales, Hypocreales, Pleosporales) can be isolated from carton. Only strains of the orders Chaetothyriales and Capnodiales are isolated from pieces of hyphae and are thus considered to have a structural function in carton construction [7,[13][14][15]. The other strains have been isolated only from spores and are most likely contaminants.…”

New and interesting chaetothyrialean fungi from Spain

“…1, 5). In the LSU tree, it clustered with low support with three strains of unidentified Chaetothyriales associated with ant galleries from a study by Nepel et al (2014). In the LSU tree, the Cladophialophora sp.…”

“…Some Chaetothyriales are abundant in humid indoor habitats (Matos et al 2002;Döğen et al 2013), but other species, by contrast, colonize harsh environments where they have to cope with drought, scarce nutrient availability, extreme temperatures and high UV-light exposure Tsuneda et al 2011). This order has also received special attention due to the recent discovery of mutualistic interactions with ant species (Voglmayr et al 2011;Nepel et al 2014), and to the ability of certain species to degrade aromatic hydrocarbon contaminants (Prenafeta-Boldú et al 2001;Badali et al 2011). …”